THE JOURNAL OF COMPARATIVE NEUROLOGY 306:39-48 (1991)
Somatosensory Cortex of the Neonatal Pig: 11. Topographic Organization of the Secondary Somatosensory Cortex (SII) SANDRA L. CRANER AND RICHARD H. RAY Department of Physiology, East Carolina University, Greenville, North Carolina 27858-4354
ABSTRACT Multiunit microelectrode recording techniques were used to delineate the somatotopic organization of the secondary somatosensory cortex (SII) of the neonatal pig. Barbiturate anesthetized piglets ranging in age from 7 days preterm to 2 months postpartum were used. The SII area, located lateral to the rostral and middle suprasylvian sulci, was found to contain a complete somatotopic representation of the contralateral body surface with a significant proportion of bilateral input for all body regions except the forehoof and forelimb. The SII forelimb and hindlimb representations were found to possess a "striplike" orientation in a rostral to caudal sequence, and the trunk representation was located posterolateral to the hindlimb representation, giving SII an inverted appearance. Two apparently separate face representations were delineated; one posterolateral to the projection from the trunk and the other anterior to the forehoof region. Unlike SI, which possesses a disproportionately large representation of the rostrum, SII has no specialized representation of the rostrum. The overall organization of SII supports the contention that this cortical region provides a more generalized representation of the entire body surface than does SI. Key words: cortical mapping, somatic sensory,localization of function, multiunit recording, ungulate
Many studies have demonstrated that the mammalian neocortex contains multiple somatosensory representations. All mammals studied to date possess at least two separate somatosensory cortices, designated as the primary somatosensory area (SI) and the secondary somatosensory area (SII). Similarities and differences in derentation, cortical representation and morphology in SI and SII have been investigated, resulting in the formation of several general rules of cortical organization and function. Both SI and SII generally receive a complete somatotopic projection from the body surface (Woolsey, '58; Whitsel, et al., '69; Werner andWhitse1, '73). However, the SI body representation is more distorted than that of SII (Nelson et al., '79), presumably reflecting the specific behavioral adaptation of the species. Also, due to larger and often bilateral receptive fields (Woolsey and Fairman, '46; Woolsey, '52; Hamuy et al., '56; Benjamin and Welker, '57; Ferrington and Rowe, '801, the body representation in SII appears less discrete than in SI. SII is contained in a relatively small patch of cortex, partly or often completely buried within fissures. As a result, it is difficult to delineate the details of the organization of the SII representation. Also, the receptive fields for SII neurons are often large and overlapping, making it difficult to determine the orientation of the body map in this cortical region.
o 1991 WILEY-LISS, INC.
The organization of SII was first described as an inverted mammunculus (Woolsey, '52, '58; Hamuy et al., '56; Lende and Woolsey, '56; T.A. Woolsey, '67; Campos and Welker, '761, with the feet pointing toward SI and the back of the trunk distal to SI. These reports were based on surface recorded evoked potentials (EPs). More recent microelectrode investigations indicate that the basic organization of the head, foot, and arm in SII is sometimes reversed, as shown for the cat (Haight, '72). In 1972, Haight suggested that SII actually has an "erect" orientation, with the feet pointing away from SI. Other investigators have found similar organizations in studies of the sheep (Johnson et al., '741, various rodents (Campos and Welker, '76; Nelson et al., '79; Pimentel-Souza et al., '801, and the raccoon (Herron, '78). Data from additional species are needed to better understand the organization of SII and traits possibly associated with variations in the organizational plan of SII. The present study and the previous work (Craner and Ray, '91) are a portion of an investigation into the perinatal development of the SI and SII areas. No study to date has compared the perinatal development of multiple somatic Accepted December 19,1990, Address reprint requests to Dr. Sandra L. Craner, who is now at the Dept. of Neurobiology, Anatomy and Cell Science, School of Medicine, University of Pittsburgh, Pittsburgh, PA 15261.
S.L. CRANER AND R.H. RAY
40 representations. The domestic pig is a suitable animal model for this series of studies due to its developmental similarities to humans (Patten, 1964; h e y , 1966). However, despite its suitability for developmental studies, the pig has not been extensively used in neurological studies. The somatosensory cortices of the pig had not been previously mapped in detail. Adrian ('43) mapped the loci of the SI rostrum representation and Woolsey and Fairman ('46) determined the loci of the SI representation for the snout and forelimb areas and the loci of the SII representation for the face, forelimb, and hindlimb areas using the evoked potential technique. However, no SII trunk representation was mapped; thus the orientation of SII was not established. The goal of the present study was to delineate the somatotopic organization of the pig SII, determining the orientation and characteristics of this cortical region.
METHODS Surgical preparation A total of 20 domestic Yorkshire pigs, ranging in age from 7 days preterm (normal gestational age = 114 days) to 2 months postpartum, were employed in this study. Preterm animals were obtained by inducing premature labor (at gestational age of 106 days) in sows with an intramuscular injection of the prostaglandin LutalyseTM(3-7 ml, depending on the weight of the sow). General anesthesia was induced by an intraperitoneal injection of sodium pentobarbital (Nembutal) (30-35 mg/ kg). Atropine (0.2 mg/kg) was injected intramuscularly to prevent excessive salivation. The trachea was cannulated and respiration maintained with a positive-pressure pump. The left femoral artery was cannulated to continuously monitor arterial pressure and the left femoral vein was cannulated for administration of drugs or fluids intravenously. Body temperature was maintained a t 38-40°C with a water circulating heating pad supplemented when necessary with an infrared heat lamp, The animal was kept hydrated with an i.v. drip of 5% dextrose in saline. Intravenous injections of sodium pentobarbital were administered to maintain a surgical level of anesthesia throughout the recording session. The head was immobilized in a stereotaxic unit (David Kopf Instruments) and a craniotomy performed, exposing the somatosensory cortices (SI and ,311) of the left hemisphere. The exposed bone margins were sealed with bone wax. Small strips of gauze soaked in a 3%agar solution were placed around the skull opening, forming a leakproof dam. The dam was then filled with warm mineral oil (38"C),thus keeping the brain warm and moist. After reflecting the dura mater, the exposed cortex was photographed. Recording sites were marked upon photographic enlargements of the cortex. At the end of every experiment the animal was given an overdose of sodium pentobarbital and perfused intracardially, first with a 0.9%saline solution, followed by a 10% formalin solution. The brain was removed and placed in 10%formalin for later histological examination.
to a micromanipulator on the stereotaxic frame. A Grass high impedance probe fed the neural signals to a Grass P5 preamplifier. A window discriminator (World Precision Instruments) was used to separate evoked activity in multiunit recordings. The neural activity was made audible through a Grass AM5 audio monitor and displayed on a Tektronix oscilloscope. Mapping procedure. Under microscopic observation, the microelectrode was lowered to the pial surface and the location of the electrode was marked on an enlarged photograph of the exposed brain. The electrode was slowly driven through the cortex with a hydraulic microdrive while the body surface was continuously palpated by hand. When a driveable cortical response was encountered, the depth of the electrode tip in the cortex was recorded and, using a small wooden probe or Semmes-Weinstein filaments, the receptive field of the response was delineated. The receptive field was then drawn on a sketch of the pig's body and the neural response characteristics were recorded. The characteristics recorded included threshold of response (low, medium, high), submodality (hair, cutaneous, joint, deep, claw), and laterality of response (bilateral, contralateral, or ipsilateral). Successive electrode penetrations were made normal to the pial surface 0.5 mm to 1 mm apart, or as close as the vascular pattern permitted. Boundaries of SII were determined by penetrations in which no driveable cells were encountered. Two or more consecutive unresponsive sites were determined at the boundaries of SII for each row of recording sites. To record from the sulci, the electrode was either driven in at an angle or a portion of the adjacent g y r u s was removed by suction, permitting easy access to the desired area. The map of the body parts within the cortex was determined by relating receptive fields to recording sites and depths of electrode penetations. The body subdivisions of SII were drawn on enlarged photographs of the brain. Composite body maps were created by overlaying the results of all the experiments and outlining the corresponding body subdivisions. It should be noted that the body subdivisions in individual animals may actually be smaller than those delineated in the composite maps due to anteroposterior shifts of the SII body representation from one animal to another.
RESULTS A total of 925 electrode penetrations were made in the SII region of 20 domestic pigs. From these penetrations 808 receptive fields were isolated. As a result, details of the SII representation of the neonatal domestic pig were revealed. The overall organization of SII is similar to that of other mammals with a complete and somatotopically organized projection from the body surface. Like many mammals, the SII representation of the pig appears inverted and bilateral receptive fields are commonly found. Additionally, multiple representations are found within SII.
Microelectrode mapping
The location and overall organization of SII
Electronics. Tungsten microelectrodes (12 megOhm) configured to favor extracellular recording from small groups of neurons and single neurons were employed. The microelectrode was attached via a hydraulic microdrive unit
The overall features of the representation of the body parts in SII of the pig as determined in this study are shown schematically in Figure 1. Located lateral to the rostra1 suprasylvian and middle suprasylvian sulci, SII occupies a
SECONDARY SOMATOSENSORY CORTEX OF THE PIGLET
41
S.L. CRANER AND R.H. RAY
42 relatively small area by comparison to the SI region (details of SI organization presented in previous work). It should be noted that the present study defines SII by electrophysiological responses to peripheral stimulation. Accordingly, the SII body representation has an inverted representation which dips into the suprasylvian sulcus. All body representations bordering the sulcus extend approximately 1.5 mm into the sulcus. The forelimb and hindlimb representations are located in strips in a rostral-caudal sequence while the trunk representation is located posterolateral to the hip representation. Two apparently separate face representations are present in this cortical region; one posterolateral to the trunk representation and one anterior to the forehoof representation. The cortical areas surrounding SII were carefully examined and, other than the SI cortical region, found to be unresponsive to cutaneous stimulation. Unresponsive zones were found in the suprasylvian sulcus between SI and SII. This may have been due to the immaturity of the cortex, and it may be necessary to study more mature pigs to fully delineate any possible transition area between SI and SII. The auditory area of the pig was not delineated.
Representation of the forelimb The forehoof (FH), foreleg (FL), and shoulder (S) have distinct areas of representation (Fig. 2A), located rostrally to caudally in strips across the cortical surface. Although separate representations are present, there is considerable overlap of these areas and the representations extend into the rostral and middle suprasylvian sulci. The distal forehoof representation is located rostrally in SII, whereas the more proximal forelimb and shoulder representations are located caudally (Fig. 2). Unlike the digit representation in some animals, a distinct progression of digit representations is not apparent in the pig. The D2 and D3 representation generally occupies most of the forehoof representation (Fig. 2B). The D1 representation tends to be located anteromedial to D2 and D3 whereas D4 generally is represented posterolaterally to D2 and D3. Most isolated digit receptive fields were located on both D2 and D3 while few receptive fields were confined to D1 and D4. (It should be noted that most recordings were from multiunit clusters and had single units been recorded, smaller receptive fields may have been delineated.) The ventral aspect of each digit is usually represented anteriorly in the corresponding digit representation while the dorsal aspect tends to be represented posteriorly. Receptive fields on the ventral pads of the forelimb usually extend entirely over one pad and sometimes over 2 or more pads. In some animals an area anterior to the digit representation received a generalized cutaneous input from the entire hoof, dorsal and ventral. However, this generalized area of representation was not present in all animals. Fewer receptive fields were isolated on the forelimb and shoulder than on the forehoof. However, like the forehoof, the ventral aspects of the forelimb and shoulder are generally located anteriorly in the representation, whereas the dorsal aspect is located posteriorly (Fig. 2B). As illustrated, receptive field size increases distally to proximally on the limb. This is a characteristic common to SII of most mammals. Of 195 receptive fields found in the forehoof representation, 70% were cutaneous and 28% were claw receptive
fields; 97% of the receptive fields were contralateral; only 3%were bilateral. In the forelimb representation, 155 receptive fields were delineated (98%were cutaneous). Of these receptive fields, 92% were contralateral and the remaining 8% were bilateral. Of 102 receptive fields found in the shoulder representation, 99% were cutaneous. However, only 87%were contralateral and 13%were bilateral in nature. The lateralities of all subrepresentations within SII are summarized in Table 1. The decrease in receptive field number, the increase in receptive field size, and the increase in bilaterality of receptive fields progressing distally to proximally on the body surface are common characteristics of the SII region of mammals.
Representation of the hindlimb The hindhoof (HH), hindlimb (HL), and hip (HI have separate areas of representation located rostrally to caudally in strips behind the shoulder representation (Fig. 3A). As with the separate body regions of the forelimb, there is considerable cortical overlap of these separate regions of the hindlimb. The entire hindlimb representation extends into the middle suprasylvian sulcus and anteriorly the hindhoof representation may overlap with the shoulder representation. As with the forehoof representation, a distinct progression of hindhoof digit representations was not found. Most isolated digit receptive fields were located on both D2 and D3. Few receptive fields were found on D1 or D4. Many receptive fields that included the ventral pads of D2 and D3 also extended over the plantar surface of the hindhoof. As with the forelimb representation, receptive fields delineated on the ventral aspect of the hind D2 and D3 were generally located anteriorly in the cortical representation, whereas receptive fields found on the dorsal aspect were generally located posteriorly. In some animals a small cortical region anterior to the D2-D3 representation received a generalized sensory input from the entire hindhoof (see Fig. 3B). However, as with the similar forehoof region, this generalized area of hindhoof representation was not present in all animals. Due to the position of the animal in the stereotaxic unit, it was difficult to stimulate the ventral surface of the hip. Therefore, this region of the pig’s body could not be adequately mapped in all animals. Similar to the hindhoof representation, the ventral aspects of the hindlimb and hip were generally located anteriorly in the corresponding cortical representation whereas the dorsal aspects were located posteriorly. Both receptive field size and degree of bilaterality increased on the more proximal hindlimb and hip. Of 83 receptive fields found in the hindhoof representation, 92% were cutaneous and the remaining 8% were excited by either hair or claw receptors; 81%of the receptive fields were contralateral and 19%were bilateral. In the hindlimb representation, 70 receptive fields were delineated (95%were cutaneous). Of these receptive fields, only 68%were strictly contralateral; 32%were bilateral. Of 80 receptive fields found in the hip representation, 91% were cutaneous, 5% were deep, and 4% were hair receptors. In addition, the degree of bilateral receptive fields was greatly increased; 41% of receptive fields were bilateral, 57% were contralateral, and 1 ipsilateral receptive field was delineated (see Table 1).
SECONDARY SOMATOSENSORY CORTEX OF THE PIGLET
D
Forehoof ~3
E
D2
43
/
i 4 b
.:4 D4
D1
7j
Fig. 2. Somatotopic organization of the SII forelimb representation. A. Location of representative penetration sites in an experimental animal. The large box is an enlargement of the cortical area outlined in the inset. FH = forehoof, FL = forelimb, S = shoulder. B. Composite forelimb representation found in all experimental animals. FH = forehoof, G = generalized forehoof input, D, = digit 1, D, = digit 2, D, = digit 3, D, = digit 4, FL, = ventral forelimb, FL, = dorsal forelimb, S, =
ventral shoulder, S, = dorsal shoulder. C. Receptive fields delineated on the contralateral and ipsilateral sides of the body. D. Receptive fields delineated on the forehoof. E. Receptive fields delineated on the ventral forelimb and shoulder. Receptive fields in C , D, and E were found at the corresponding penetration sites in A. Receptive fields alphabetically labeled (e.g. 16a, 16b, 16c) were found at progressively greater depths in the penetration site.
S.L. CRANER AND R.H. RAY
44 TABLE 1. Summary of Lateralitiesin Subrepresentationsof the Neonatal Pig SII Cortical representation Forehoof Forelimb Shoulder Hindhoof Hindlimb Hip Trunk Face
%
%
Contralateral
Bilateral
97 92 87 81 68
3 8 13
57 59 65
19 32 41 38 34
9% Ipsilateral -
-
2
3 1
found in all animals. Some animals displayed only one of the two areas, or occassionally only a few receptive fields were delineated in one of the representations. Of 98 receptive fields obtained from the face, 34% were bilateral, 65%were contralateral, and 1 receptive field was ipsilateral. In addition, 92% of these receptive fields were cutaneous. Only 5 receptive fields on the rostrum were delineated in 3 animals, and 12 receptive fields in the mouth were delineated in 5 animals. The receptive fields found in the mouth and on the rostrum exhibited approximately the same degree of bilaterality as that found on the face (Table 1).
Representation of the trunk The trunk representation of the pig is located directly posterolaterally to the hip representation. In 16 animals, 86 receptive fields were delineated on the trunk. In a few animals, a trunk region was not found, whereas other animals had a comparatively large trunk representation with as many as 6-16 receptive fields delineated. Due to the position of the animal in the stereotaxic unit, it was difficult to stimulate the ventral abdomen and chest. Therefore, these representations could not be well mapped. However, receptive fields were delineated on the dorsal back, sides, and tail of the animal. As shown in the composite drawing of the trunk region (Fig. 4B), the trunk representation curves around the hindlimb representation. The posterior portion of the trunk is represented medially along and slightly into the sulcus, and the more anterior regions of the trunk are represented more laterally on the cortical surface. In addition, the ventral aspect of the trunk is located more anteriorly in the representation and the dorsal aspect is found posteriorly. The receptive fields on the trunk were usually much larger than those found on the limbs and face of the animal. Additionally,the trunk representation exhibited many bilateral receptive fields, including those extending across the midline. Of the trunk receptive fields, 38% were bilateral, 59%were contralateral, and 2 receptive fields were strictly ipsilateral. Only 3 hair receptive fields were found on the trunk; the remaining receptive fields were cutaneous. The increase in receptive field size and increased degree of bilaterality on the trunk of the animal are other characteristics consistent with the SII representations of other mammals.
Representation of the face The forelimb, hindlimb, and trunk representations are surrounded posterolaterally and anteriorly by cortical areas receiving afferent information from the face of the pig. The two face areas seem to be separate and distinct representations (Fig. 5). A composite of the face areas found in 15 animals is presented in Figure 5B. No apparent difference in receptive field areas or laterality of input in the two representations was detected. Although it remains possible that F, is an extension of F,, no distinct connection was mapped between the two areas. Isolated receptive fields in the SII face representations were primarily located on the outer surfaces of the face-the chin, cheek, jowl, ear, and neck. Few receptive fields were found in the mouth or on the rostrum of the animal. It should be noted that the scalp of the animal could not be stimulated due to the craniotomy; therefore no scalp representation could be mapped. A certain amount of variability was present in the face representations. Both SII face representations were not
DISCUSSION This study provides a detailed micromap of SII of the neonatal pig. Several features of the overall organization of the pig SII are similar to those described for other mammals. A complete body map is present and bilateral receptive fields are relatively common. Progressing distally to proximally on the limbs and trunk, the receptive field size increases, the receptive field number decreases, and the degree of bilaterality increases. The pig SII also is a much less distorted peripheral representation than is SI. Unlike SI (Adrian, '43; Woolsey and Fairman, '46; Craner and Ray, '86, '911, the SII region contains no specialized rostrum representation. Each individual body part has a well proportioned representation. An interesting aspect of the pig SII region is the presence of 2 apparently separate face regions. The SII region of the cat also contains multiple representations; it has 2 representations of the distal forelimb and hindlimb (Burton et al., '82). The 2 separate face regions found in the pig SII may therefore reflect functional similarities to the cat cortex. Alternatively, the 2 face representations of the pig SII may actually be continuous laterally forming one enlarged face region encircling the other body representations. For most mammals, parts of the face are an important sensory surface and an enlarged SII head representation appears in the tree shrew (Sur et al., '811, the grey squirrel (Nelson et al., '791, and the opossum (Pubols, '77). The enlarged SII face representation may be a common feature and the 2 face regions delineated in the neonatal pig may actually reflect one enlarged region. Another possible explanation for the presence of the posterior face representation (F,) is that this second representation may not be a part of the SII representation, but rather an area homologous to the SIV region of the cat. It has been suggested that one of the multiple representations found in the cat SII may actually be a portion of the SW representation described by Clemo and Stein ('82, '83). Because microelectrode penetrations into the region of SII might pass through various cortical regions, the somatosensory responses alone cannot define the position or extent of SII. Since the cytoarchitectural development of the neonatal piglets employed in this study was too immature to sufficiently determine classical cytoarchitectural differences in somatosensory fields, further cytoarchitectural and physiological studies need to be conducted in mature pigs to determine whether the pig F, area is indeed part of an extended SII representation or actually a separate field. As previously stated, a controversy exists regarding the orientation of the body representation of SII. In cats, Woolsey and Fairman ('46) determined that the forelimb digits point toward, whereas Haight ('72) concluded that
45
SECONDARY SOMATOSENSORY CORTEX OF THE PIGLET
FL
D
D4
Hind hoof D3
E
D2
D1
Forehoof D3
D2
D4
Fig. 3. Somatotopic organization of the SII hindlimb representation. A. Location of representative penetration sites in an experimental animal. HH = hindhoof, HL = hindlimb, H = hip. B. Composite representation found in all experimental animals. FL = forelimb, G = generalized from hindhoof, D, = digit 2, D, = digit 3, HLv = ventral .~ . _ innut ~ ~ hindlimb, k L d = dorsal hindlimb, H; = ventral hip, Hd = dorsal hip. ~
D1
C. Receptive fields delineated on the contralateral and ipsilateral sides of the body. D. Receptive fields delineated on the hindhoof. E. Receptive fields delineated on the forehoof. F. Receptive field in the upper mouth. Receptive fields illustrated in C , D, E, and F were found at the corresponding penetration sites in A.
S.L. CRANER AND R.H. RAY
46
Forehoof D3
04
E
D2
D1
Fig. 4. Somatotopic organization ofthe SII trunk representation. A. Location of representative penetration sites in an experimental animal. T = trunk representation. B. Composite representation found in all experimental animals. FL = forelimb, HL = hindlimb, T, = ventral trunk, T, = dorsal trunk, Post. = posterior trunk representation located medially, Ant. = anterior trunk representation located laterally.
C. Receptive fields delineated on the contralateral and ipsilateral sides of the body. D. Receptive fields delineated on the forehoof. E.Receptive fields delineated on the ventral forelimb and shoulder. Receptive fields illustrated in C, D, and E were found at the corresponding penetration sitesinA.
SECONDARY SOMATOSENSORY CORTEX OF THE PIGLET
D
Hindhoof D3
E
D2
Forehoof D3
47
F
D2
+5,7
D4
Di
D4
D1
\-
Fig. 5. Somatotopic organization of the SII face representations. A. Location of representative penetration sites in an experimental animal. F,= anterior face representation, F, = posterior face representation. B. Composite representation found in all experimental animals. FL = forelimb, HL = hindlimb, T = trunk. C. Receptive fields delineated on
the contralateral and ipsilateral sides of the body. D. Receptive fields delineated on the hindhoof. E. Receptive fields delineated on the forehoof. F. Receptive fields found on the ventral shoulder. Receptive fields illustrated in C, D, E, and F were found at the corresponding penetration sites in A. Receptive field 12b in Fig. 5F was bilateral.
S.L. CRANER AND R.H. RAY
48 they point away from, the anterior suprasylvian sulcus. According to Burton and Robinson (’81),it is possible, however, to interpret the cat SII as having a striplike organization, similar to the map seen in the monkey, in which the limbs follow oblique anterior to posterior “nested strips” across SII (Burton and Robinson, ’81). This “dermatomal-strip” organization is similar to that found in our study of the pig SII cortex. The digits and limbs do not point toward or away from the suprasylvian sulcus, but are represented in anterior t o posterior nested strips across SII. The trunk representation seems to curve posterolaterally to the digit and limb representations, thus giving the pig SII what can be considered to be an inverted organization. Like the pig, the sheep and llama are members of the Arteriodactyla order. The llama, a member of the suborder Tylopoda, has an inverted SII (Welker et al., ’76),similar to that of the pig, a member of the suborder Suiformes. Sheep, however, members of the suborder Ruminantia, demonstrate an erect SII region (Johnson et al., ’74). These findings indicate that dissimilar cortical plans of organization can exist in mammals of the same order. In contrast, the SII representations of the sheep and llama may need to be reexamined to determine whether a dermatomal-like organization is present, thereby resolving the disparate portrayals of SII organization. It has been suggested that SI may be a cortical region primarily devoted to a complex representation of specialized areas specific to each species’ behavioral adaptations, whereas SII may provide a more complete generalized representation of the entire body surface. Evidence from our studies supports this idea. The SII trunk and hindlimb representations were larger, better defined, and had a more regular progression of receptive fields than the corresponding representations in SI. SII also had a more generalized input from the face, primarily from the lower cheeks, chin, jaw, and ear. Few receptive fields in the mouth were found and no specialized representation of the rostrum was present in SII. By contrast, SI contained very elaborate rostrum and face representations that received input from the entire face and head, including the mouth, lips, and tongue. The SI trunk and hindlimb representations were poorly developed and there was a great deal of overlap in the forehoof, foreleg, and shoulder representations. These facts support the idea that SII provides a more generalized representation of the entire body surface, whereas SI is a more specialized body representation reflecting the behavioral adaptation of the animal.
ACKNOWLEDGMENTS We would like to thank Alan Branigan and the East Carolina University Center for Health Sciences Communications for their help with the illustrations. Partial support of this work was provided by Sigma Xi, the Scientific Research Society.
LITERATURE CITED Adrian, E.D. (1943) Afferent areas in the brain of ungulates. Brain 66:89103. Arey, L.B. (1966) Developmental Anatomy. Philadelphia: W.B. Saunders Co.
Benjamin, R.M., and W.I. Welker (1957) Somatic receivingareas of cerebral cortex of squirrel monkey (Samiri sciureus). J. Neurophysiol. 20~286299. Burton, H., and C.J. Robinson (1981)Organization of the SII parietal cortex: Multiple somatic sensory representations within and near the second somatic sensory area of cynomologus monkeys. In C.N. Woolsey (ed): Cortical Sensory Organization, Vol 1: Multiple Somatic Areas. Clifton, NJ: Humana Press, pp. 67-119. Burton, H., G. Mitchell, and D. Brent (1982) Second somatic sensory area in the cerebral cortex of cats: Somatotopic organization and cytoarchitecture. J. Comp. Neurol. 210;109-135. Campos, G.B., and W.I. Welker (1976) Comparisons between brains of a large and a small hystricomorph rodent capybara, Hydrochoerus, and guinea pig, Cauis: Neocortical projection regions and measurements of brain subdivisions. Brain Behav. and Evol. 13:243-266. Clemo, H.R., and B.E. Stein (1982) Somatosensory cortex: a ‘new’ somatotopic representation. Brain Research 235:162-168. Clemo, H.R., and B.E. Stein (1983) Organization of a fourth somatosensory area of cortex in cat. J. Neurophys. 50~910-925. Craner, S.L., and R.H. Ray (19861 Topographic organization of somatosensory cortices SI and SII of the neonatal pig. Physiologist 29t120. Craner, S.L., and R.H. Ray (1991) Somatosensory cortex of the neonatal pig: I. Topographic organization of the primary somatosensory cortex (SI).J. Comp. Neurol. 306:24-38. Ferrington, D.G., and M.J. Rowe (1980) Differential contributions to coding of cutaneous vibratory information by cortical somatosensory areas I and 11. J. Neurophysiol. 43:310-331. Haight, J.R. (1972) The general organization of somatotopic projections to SII cerebral neocortex in the cat. Brain Res. 44:483-502. Hamuy, T.P., R.B. Bromiley, and C.N. Woolsey (1956) Somatic afferent areas I and I1 of dog’s cerebral cortex. J. Neurophysiol. 19:485-499. Herron, P. (1978) The organization of somatotopic projections to S-I1 cerebral neocortex in the raccoon (Procyon btor). J. Comp. Neurol. 181:717-728. Johnson, J.I., E.W. Rubel, and G.I. Hatton (1974) Mechanosensory projections to cerebral cortex of sheep. J. Comp. Neurol. 158:81-106. Lende, R.A., and C.N. Woolsey (1956) Sensory and motor localization in cerebral cortex of porcupine (Erethizon dorsatum). J. Neurophysiol. 19:544-63. Nelson, R.J., M. Sur, and J.H. Kaas (1979) The organization of the second somatosensory area (SmII) of grey squirrel. J. Comp. Neurol. 184:473490. Patten, B.M. (1964) Foundations of Embryology, 2nd ed. New York: McGraw-Hill. Pimentel-Souza, F., R.M. Cosenza, G.B. Campos, and J.I. Johnson (1980) Somatic sensory cortical regions of the Agouti (Dasyprota Aguti). Brain Behav. Evol. 17,218-240. Pubols, B.H. 11977) The second somatic sensory area (SmII) of opossum neocortex. J. Comp. Neurol. 174:71-78. Sur, M., R. Weller, and J.H. G a s . (1981) The organization ofthe somatosensory area I1 in tree shrews. J. Comp. Neurol. 201:121-133. Welker, W.I., H.O. Adrian, W. Lifschitz, R. Kaulen, E. Caviedes, and W. Gutman (1976) Somatic sensory cortex of llama (Lama glama). Brain Behav. Evol. 13:284-295. Werner, G., and B.L. Whitsel (1973) Functional organization of the somatosensory cortex. In: A. Iggo (ed): Handbook of Sensory Physiology, Vol. 11. New York: Springer, pp. 621-700. Whitsel, B.L., L.M. Petrucelli, and G. Werner (1969) Symmetry and connectivity in the map of the body surface in somatosensory Area I1 of primates. J. Neurophysiol. 32.1 70-183. Woolsey, C.N. (1952) Patterns of localization in sensory and motor areas of the cerebral cortex. In: Milbank Symposium. The Biology of Mental Health and Disease, Chap. 14. New York: Hoeber, pp. 193-206. Woolsey, C.N. (1958) Organization of somatic sensory and motor areas of the cerebral cortex. In: H.F. Harlow and C.N. Woolsey (eds): Biological and Biochemical Bases of Behavior. Madison: University of Wisconsin Press, pp. 63-81. Woolsey, C.N., and D. Fairman (1946) Contralateral, ipsilateral and bilateral representation of cutaneous receptors in somatic areas I and I1 of the cerebral cortex of pig, sheep and other mammals. Surgery 19:684-702. Woolsey, T.A. (1967) Somatosensory, auditory and visual cortical areas of the mouse. John Hopkins Med. J. 121:91-112.
Somatosensory Cortex of the Neonatal Pig: 11. Topographic Organization of the Secondary Somatosensory Cortex (SII) SANDRA L. CRANER AND RICHARD H. RAY Department of Physiology, East Carolina University, Greenville, North Carolina 27858-4354
ABSTRACT Multiunit microelectrode recording techniques were used to delineate the somatotopic organization of the secondary somatosensory cortex (SII) of the neonatal pig. Barbiturate anesthetized piglets ranging in age from 7 days preterm to 2 months postpartum were used. The SII area, located lateral to the rostral and middle suprasylvian sulci, was found to contain a complete somatotopic representation of the contralateral body surface with a significant proportion of bilateral input for all body regions except the forehoof and forelimb. The SII forelimb and hindlimb representations were found to possess a "striplike" orientation in a rostral to caudal sequence, and the trunk representation was located posterolateral to the hindlimb representation, giving SII an inverted appearance. Two apparently separate face representations were delineated; one posterolateral to the projection from the trunk and the other anterior to the forehoof region. Unlike SI, which possesses a disproportionately large representation of the rostrum, SII has no specialized representation of the rostrum. The overall organization of SII supports the contention that this cortical region provides a more generalized representation of the entire body surface than does SI. Key words: cortical mapping, somatic sensory,localization of function, multiunit recording, ungulate
Many studies have demonstrated that the mammalian neocortex contains multiple somatosensory representations. All mammals studied to date possess at least two separate somatosensory cortices, designated as the primary somatosensory area (SI) and the secondary somatosensory area (SII). Similarities and differences in derentation, cortical representation and morphology in SI and SII have been investigated, resulting in the formation of several general rules of cortical organization and function. Both SI and SII generally receive a complete somatotopic projection from the body surface (Woolsey, '58; Whitsel, et al., '69; Werner andWhitse1, '73). However, the SI body representation is more distorted than that of SII (Nelson et al., '79), presumably reflecting the specific behavioral adaptation of the species. Also, due to larger and often bilateral receptive fields (Woolsey and Fairman, '46; Woolsey, '52; Hamuy et al., '56; Benjamin and Welker, '57; Ferrington and Rowe, '801, the body representation in SII appears less discrete than in SI. SII is contained in a relatively small patch of cortex, partly or often completely buried within fissures. As a result, it is difficult to delineate the details of the organization of the SII representation. Also, the receptive fields for SII neurons are often large and overlapping, making it difficult to determine the orientation of the body map in this cortical region.
o 1991 WILEY-LISS, INC.
The organization of SII was first described as an inverted mammunculus (Woolsey, '52, '58; Hamuy et al., '56; Lende and Woolsey, '56; T.A. Woolsey, '67; Campos and Welker, '761, with the feet pointing toward SI and the back of the trunk distal to SI. These reports were based on surface recorded evoked potentials (EPs). More recent microelectrode investigations indicate that the basic organization of the head, foot, and arm in SII is sometimes reversed, as shown for the cat (Haight, '72). In 1972, Haight suggested that SII actually has an "erect" orientation, with the feet pointing away from SI. Other investigators have found similar organizations in studies of the sheep (Johnson et al., '741, various rodents (Campos and Welker, '76; Nelson et al., '79; Pimentel-Souza et al., '801, and the raccoon (Herron, '78). Data from additional species are needed to better understand the organization of SII and traits possibly associated with variations in the organizational plan of SII. The present study and the previous work (Craner and Ray, '91) are a portion of an investigation into the perinatal development of the SI and SII areas. No study to date has compared the perinatal development of multiple somatic Accepted December 19,1990, Address reprint requests to Dr. Sandra L. Craner, who is now at the Dept. of Neurobiology, Anatomy and Cell Science, School of Medicine, University of Pittsburgh, Pittsburgh, PA 15261.
S.L. CRANER AND R.H. RAY
40 representations. The domestic pig is a suitable animal model for this series of studies due to its developmental similarities to humans (Patten, 1964; h e y , 1966). However, despite its suitability for developmental studies, the pig has not been extensively used in neurological studies. The somatosensory cortices of the pig had not been previously mapped in detail. Adrian ('43) mapped the loci of the SI rostrum representation and Woolsey and Fairman ('46) determined the loci of the SI representation for the snout and forelimb areas and the loci of the SII representation for the face, forelimb, and hindlimb areas using the evoked potential technique. However, no SII trunk representation was mapped; thus the orientation of SII was not established. The goal of the present study was to delineate the somatotopic organization of the pig SII, determining the orientation and characteristics of this cortical region.
METHODS Surgical preparation A total of 20 domestic Yorkshire pigs, ranging in age from 7 days preterm (normal gestational age = 114 days) to 2 months postpartum, were employed in this study. Preterm animals were obtained by inducing premature labor (at gestational age of 106 days) in sows with an intramuscular injection of the prostaglandin LutalyseTM(3-7 ml, depending on the weight of the sow). General anesthesia was induced by an intraperitoneal injection of sodium pentobarbital (Nembutal) (30-35 mg/ kg). Atropine (0.2 mg/kg) was injected intramuscularly to prevent excessive salivation. The trachea was cannulated and respiration maintained with a positive-pressure pump. The left femoral artery was cannulated to continuously monitor arterial pressure and the left femoral vein was cannulated for administration of drugs or fluids intravenously. Body temperature was maintained a t 38-40°C with a water circulating heating pad supplemented when necessary with an infrared heat lamp, The animal was kept hydrated with an i.v. drip of 5% dextrose in saline. Intravenous injections of sodium pentobarbital were administered to maintain a surgical level of anesthesia throughout the recording session. The head was immobilized in a stereotaxic unit (David Kopf Instruments) and a craniotomy performed, exposing the somatosensory cortices (SI and ,311) of the left hemisphere. The exposed bone margins were sealed with bone wax. Small strips of gauze soaked in a 3%agar solution were placed around the skull opening, forming a leakproof dam. The dam was then filled with warm mineral oil (38"C),thus keeping the brain warm and moist. After reflecting the dura mater, the exposed cortex was photographed. Recording sites were marked upon photographic enlargements of the cortex. At the end of every experiment the animal was given an overdose of sodium pentobarbital and perfused intracardially, first with a 0.9%saline solution, followed by a 10% formalin solution. The brain was removed and placed in 10%formalin for later histological examination.
to a micromanipulator on the stereotaxic frame. A Grass high impedance probe fed the neural signals to a Grass P5 preamplifier. A window discriminator (World Precision Instruments) was used to separate evoked activity in multiunit recordings. The neural activity was made audible through a Grass AM5 audio monitor and displayed on a Tektronix oscilloscope. Mapping procedure. Under microscopic observation, the microelectrode was lowered to the pial surface and the location of the electrode was marked on an enlarged photograph of the exposed brain. The electrode was slowly driven through the cortex with a hydraulic microdrive while the body surface was continuously palpated by hand. When a driveable cortical response was encountered, the depth of the electrode tip in the cortex was recorded and, using a small wooden probe or Semmes-Weinstein filaments, the receptive field of the response was delineated. The receptive field was then drawn on a sketch of the pig's body and the neural response characteristics were recorded. The characteristics recorded included threshold of response (low, medium, high), submodality (hair, cutaneous, joint, deep, claw), and laterality of response (bilateral, contralateral, or ipsilateral). Successive electrode penetrations were made normal to the pial surface 0.5 mm to 1 mm apart, or as close as the vascular pattern permitted. Boundaries of SII were determined by penetrations in which no driveable cells were encountered. Two or more consecutive unresponsive sites were determined at the boundaries of SII for each row of recording sites. To record from the sulci, the electrode was either driven in at an angle or a portion of the adjacent g y r u s was removed by suction, permitting easy access to the desired area. The map of the body parts within the cortex was determined by relating receptive fields to recording sites and depths of electrode penetations. The body subdivisions of SII were drawn on enlarged photographs of the brain. Composite body maps were created by overlaying the results of all the experiments and outlining the corresponding body subdivisions. It should be noted that the body subdivisions in individual animals may actually be smaller than those delineated in the composite maps due to anteroposterior shifts of the SII body representation from one animal to another.
RESULTS A total of 925 electrode penetrations were made in the SII region of 20 domestic pigs. From these penetrations 808 receptive fields were isolated. As a result, details of the SII representation of the neonatal domestic pig were revealed. The overall organization of SII is similar to that of other mammals with a complete and somatotopically organized projection from the body surface. Like many mammals, the SII representation of the pig appears inverted and bilateral receptive fields are commonly found. Additionally, multiple representations are found within SII.
Microelectrode mapping
The location and overall organization of SII
Electronics. Tungsten microelectrodes (12 megOhm) configured to favor extracellular recording from small groups of neurons and single neurons were employed. The microelectrode was attached via a hydraulic microdrive unit
The overall features of the representation of the body parts in SII of the pig as determined in this study are shown schematically in Figure 1. Located lateral to the rostra1 suprasylvian and middle suprasylvian sulci, SII occupies a
SECONDARY SOMATOSENSORY CORTEX OF THE PIGLET
41
S.L. CRANER AND R.H. RAY
42 relatively small area by comparison to the SI region (details of SI organization presented in previous work). It should be noted that the present study defines SII by electrophysiological responses to peripheral stimulation. Accordingly, the SII body representation has an inverted representation which dips into the suprasylvian sulcus. All body representations bordering the sulcus extend approximately 1.5 mm into the sulcus. The forelimb and hindlimb representations are located in strips in a rostral-caudal sequence while the trunk representation is located posterolateral to the hip representation. Two apparently separate face representations are present in this cortical region; one posterolateral to the trunk representation and one anterior to the forehoof representation. The cortical areas surrounding SII were carefully examined and, other than the SI cortical region, found to be unresponsive to cutaneous stimulation. Unresponsive zones were found in the suprasylvian sulcus between SI and SII. This may have been due to the immaturity of the cortex, and it may be necessary to study more mature pigs to fully delineate any possible transition area between SI and SII. The auditory area of the pig was not delineated.
Representation of the forelimb The forehoof (FH), foreleg (FL), and shoulder (S) have distinct areas of representation (Fig. 2A), located rostrally to caudally in strips across the cortical surface. Although separate representations are present, there is considerable overlap of these areas and the representations extend into the rostral and middle suprasylvian sulci. The distal forehoof representation is located rostrally in SII, whereas the more proximal forelimb and shoulder representations are located caudally (Fig. 2). Unlike the digit representation in some animals, a distinct progression of digit representations is not apparent in the pig. The D2 and D3 representation generally occupies most of the forehoof representation (Fig. 2B). The D1 representation tends to be located anteromedial to D2 and D3 whereas D4 generally is represented posterolaterally to D2 and D3. Most isolated digit receptive fields were located on both D2 and D3 while few receptive fields were confined to D1 and D4. (It should be noted that most recordings were from multiunit clusters and had single units been recorded, smaller receptive fields may have been delineated.) The ventral aspect of each digit is usually represented anteriorly in the corresponding digit representation while the dorsal aspect tends to be represented posteriorly. Receptive fields on the ventral pads of the forelimb usually extend entirely over one pad and sometimes over 2 or more pads. In some animals an area anterior to the digit representation received a generalized cutaneous input from the entire hoof, dorsal and ventral. However, this generalized area of representation was not present in all animals. Fewer receptive fields were isolated on the forelimb and shoulder than on the forehoof. However, like the forehoof, the ventral aspects of the forelimb and shoulder are generally located anteriorly in the representation, whereas the dorsal aspect is located posteriorly (Fig. 2B). As illustrated, receptive field size increases distally to proximally on the limb. This is a characteristic common to SII of most mammals. Of 195 receptive fields found in the forehoof representation, 70% were cutaneous and 28% were claw receptive
fields; 97% of the receptive fields were contralateral; only 3%were bilateral. In the forelimb representation, 155 receptive fields were delineated (98%were cutaneous). Of these receptive fields, 92% were contralateral and the remaining 8% were bilateral. Of 102 receptive fields found in the shoulder representation, 99% were cutaneous. However, only 87%were contralateral and 13%were bilateral in nature. The lateralities of all subrepresentations within SII are summarized in Table 1. The decrease in receptive field number, the increase in receptive field size, and the increase in bilaterality of receptive fields progressing distally to proximally on the body surface are common characteristics of the SII region of mammals.
Representation of the hindlimb The hindhoof (HH), hindlimb (HL), and hip (HI have separate areas of representation located rostrally to caudally in strips behind the shoulder representation (Fig. 3A). As with the separate body regions of the forelimb, there is considerable cortical overlap of these separate regions of the hindlimb. The entire hindlimb representation extends into the middle suprasylvian sulcus and anteriorly the hindhoof representation may overlap with the shoulder representation. As with the forehoof representation, a distinct progression of hindhoof digit representations was not found. Most isolated digit receptive fields were located on both D2 and D3. Few receptive fields were found on D1 or D4. Many receptive fields that included the ventral pads of D2 and D3 also extended over the plantar surface of the hindhoof. As with the forelimb representation, receptive fields delineated on the ventral aspect of the hind D2 and D3 were generally located anteriorly in the cortical representation, whereas receptive fields found on the dorsal aspect were generally located posteriorly. In some animals a small cortical region anterior to the D2-D3 representation received a generalized sensory input from the entire hindhoof (see Fig. 3B). However, as with the similar forehoof region, this generalized area of hindhoof representation was not present in all animals. Due to the position of the animal in the stereotaxic unit, it was difficult to stimulate the ventral surface of the hip. Therefore, this region of the pig’s body could not be adequately mapped in all animals. Similar to the hindhoof representation, the ventral aspects of the hindlimb and hip were generally located anteriorly in the corresponding cortical representation whereas the dorsal aspects were located posteriorly. Both receptive field size and degree of bilaterality increased on the more proximal hindlimb and hip. Of 83 receptive fields found in the hindhoof representation, 92% were cutaneous and the remaining 8% were excited by either hair or claw receptors; 81%of the receptive fields were contralateral and 19%were bilateral. In the hindlimb representation, 70 receptive fields were delineated (95%were cutaneous). Of these receptive fields, only 68%were strictly contralateral; 32%were bilateral. Of 80 receptive fields found in the hip representation, 91% were cutaneous, 5% were deep, and 4% were hair receptors. In addition, the degree of bilateral receptive fields was greatly increased; 41% of receptive fields were bilateral, 57% were contralateral, and 1 ipsilateral receptive field was delineated (see Table 1).
SECONDARY SOMATOSENSORY CORTEX OF THE PIGLET
D
Forehoof ~3
E
D2
43
/
i 4 b
.:4 D4
D1
7j
Fig. 2. Somatotopic organization of the SII forelimb representation. A. Location of representative penetration sites in an experimental animal. The large box is an enlargement of the cortical area outlined in the inset. FH = forehoof, FL = forelimb, S = shoulder. B. Composite forelimb representation found in all experimental animals. FH = forehoof, G = generalized forehoof input, D, = digit 1, D, = digit 2, D, = digit 3, D, = digit 4, FL, = ventral forelimb, FL, = dorsal forelimb, S, =
ventral shoulder, S, = dorsal shoulder. C. Receptive fields delineated on the contralateral and ipsilateral sides of the body. D. Receptive fields delineated on the forehoof. E. Receptive fields delineated on the ventral forelimb and shoulder. Receptive fields in C , D, and E were found at the corresponding penetration sites in A. Receptive fields alphabetically labeled (e.g. 16a, 16b, 16c) were found at progressively greater depths in the penetration site.
S.L. CRANER AND R.H. RAY
44 TABLE 1. Summary of Lateralitiesin Subrepresentationsof the Neonatal Pig SII Cortical representation Forehoof Forelimb Shoulder Hindhoof Hindlimb Hip Trunk Face
%
%
Contralateral
Bilateral
97 92 87 81 68
3 8 13
57 59 65
19 32 41 38 34
9% Ipsilateral -
-
2
3 1
found in all animals. Some animals displayed only one of the two areas, or occassionally only a few receptive fields were delineated in one of the representations. Of 98 receptive fields obtained from the face, 34% were bilateral, 65%were contralateral, and 1 receptive field was ipsilateral. In addition, 92% of these receptive fields were cutaneous. Only 5 receptive fields on the rostrum were delineated in 3 animals, and 12 receptive fields in the mouth were delineated in 5 animals. The receptive fields found in the mouth and on the rostrum exhibited approximately the same degree of bilaterality as that found on the face (Table 1).
Representation of the trunk The trunk representation of the pig is located directly posterolaterally to the hip representation. In 16 animals, 86 receptive fields were delineated on the trunk. In a few animals, a trunk region was not found, whereas other animals had a comparatively large trunk representation with as many as 6-16 receptive fields delineated. Due to the position of the animal in the stereotaxic unit, it was difficult to stimulate the ventral abdomen and chest. Therefore, these representations could not be well mapped. However, receptive fields were delineated on the dorsal back, sides, and tail of the animal. As shown in the composite drawing of the trunk region (Fig. 4B), the trunk representation curves around the hindlimb representation. The posterior portion of the trunk is represented medially along and slightly into the sulcus, and the more anterior regions of the trunk are represented more laterally on the cortical surface. In addition, the ventral aspect of the trunk is located more anteriorly in the representation and the dorsal aspect is found posteriorly. The receptive fields on the trunk were usually much larger than those found on the limbs and face of the animal. Additionally,the trunk representation exhibited many bilateral receptive fields, including those extending across the midline. Of the trunk receptive fields, 38% were bilateral, 59%were contralateral, and 2 receptive fields were strictly ipsilateral. Only 3 hair receptive fields were found on the trunk; the remaining receptive fields were cutaneous. The increase in receptive field size and increased degree of bilaterality on the trunk of the animal are other characteristics consistent with the SII representations of other mammals.
Representation of the face The forelimb, hindlimb, and trunk representations are surrounded posterolaterally and anteriorly by cortical areas receiving afferent information from the face of the pig. The two face areas seem to be separate and distinct representations (Fig. 5). A composite of the face areas found in 15 animals is presented in Figure 5B. No apparent difference in receptive field areas or laterality of input in the two representations was detected. Although it remains possible that F, is an extension of F,, no distinct connection was mapped between the two areas. Isolated receptive fields in the SII face representations were primarily located on the outer surfaces of the face-the chin, cheek, jowl, ear, and neck. Few receptive fields were found in the mouth or on the rostrum of the animal. It should be noted that the scalp of the animal could not be stimulated due to the craniotomy; therefore no scalp representation could be mapped. A certain amount of variability was present in the face representations. Both SII face representations were not
DISCUSSION This study provides a detailed micromap of SII of the neonatal pig. Several features of the overall organization of the pig SII are similar to those described for other mammals. A complete body map is present and bilateral receptive fields are relatively common. Progressing distally to proximally on the limbs and trunk, the receptive field size increases, the receptive field number decreases, and the degree of bilaterality increases. The pig SII also is a much less distorted peripheral representation than is SI. Unlike SI (Adrian, '43; Woolsey and Fairman, '46; Craner and Ray, '86, '911, the SII region contains no specialized rostrum representation. Each individual body part has a well proportioned representation. An interesting aspect of the pig SII region is the presence of 2 apparently separate face regions. The SII region of the cat also contains multiple representations; it has 2 representations of the distal forelimb and hindlimb (Burton et al., '82). The 2 separate face regions found in the pig SII may therefore reflect functional similarities to the cat cortex. Alternatively, the 2 face representations of the pig SII may actually be continuous laterally forming one enlarged face region encircling the other body representations. For most mammals, parts of the face are an important sensory surface and an enlarged SII head representation appears in the tree shrew (Sur et al., '811, the grey squirrel (Nelson et al., '791, and the opossum (Pubols, '77). The enlarged SII face representation may be a common feature and the 2 face regions delineated in the neonatal pig may actually reflect one enlarged region. Another possible explanation for the presence of the posterior face representation (F,) is that this second representation may not be a part of the SII representation, but rather an area homologous to the SIV region of the cat. It has been suggested that one of the multiple representations found in the cat SII may actually be a portion of the SW representation described by Clemo and Stein ('82, '83). Because microelectrode penetrations into the region of SII might pass through various cortical regions, the somatosensory responses alone cannot define the position or extent of SII. Since the cytoarchitectural development of the neonatal piglets employed in this study was too immature to sufficiently determine classical cytoarchitectural differences in somatosensory fields, further cytoarchitectural and physiological studies need to be conducted in mature pigs to determine whether the pig F, area is indeed part of an extended SII representation or actually a separate field. As previously stated, a controversy exists regarding the orientation of the body representation of SII. In cats, Woolsey and Fairman ('46) determined that the forelimb digits point toward, whereas Haight ('72) concluded that
45
SECONDARY SOMATOSENSORY CORTEX OF THE PIGLET
FL
D
D4
Hind hoof D3
E
D2
D1
Forehoof D3
D2
D4
Fig. 3. Somatotopic organization of the SII hindlimb representation. A. Location of representative penetration sites in an experimental animal. HH = hindhoof, HL = hindlimb, H = hip. B. Composite representation found in all experimental animals. FL = forelimb, G = generalized from hindhoof, D, = digit 2, D, = digit 3, HLv = ventral .~ . _ innut ~ ~ hindlimb, k L d = dorsal hindlimb, H; = ventral hip, Hd = dorsal hip. ~
D1
C. Receptive fields delineated on the contralateral and ipsilateral sides of the body. D. Receptive fields delineated on the hindhoof. E. Receptive fields delineated on the forehoof. F. Receptive field in the upper mouth. Receptive fields illustrated in C , D, E, and F were found at the corresponding penetration sites in A.
S.L. CRANER AND R.H. RAY
46
Forehoof D3
04
E
D2
D1
Fig. 4. Somatotopic organization ofthe SII trunk representation. A. Location of representative penetration sites in an experimental animal. T = trunk representation. B. Composite representation found in all experimental animals. FL = forelimb, HL = hindlimb, T, = ventral trunk, T, = dorsal trunk, Post. = posterior trunk representation located medially, Ant. = anterior trunk representation located laterally.
C. Receptive fields delineated on the contralateral and ipsilateral sides of the body. D. Receptive fields delineated on the forehoof. E.Receptive fields delineated on the ventral forelimb and shoulder. Receptive fields illustrated in C, D, and E were found at the corresponding penetration sitesinA.
SECONDARY SOMATOSENSORY CORTEX OF THE PIGLET
D
Hindhoof D3
E
D2
Forehoof D3
47
F
D2
+5,7
D4
Di
D4
D1
\-
Fig. 5. Somatotopic organization of the SII face representations. A. Location of representative penetration sites in an experimental animal. F,= anterior face representation, F, = posterior face representation. B. Composite representation found in all experimental animals. FL = forelimb, HL = hindlimb, T = trunk. C. Receptive fields delineated on
the contralateral and ipsilateral sides of the body. D. Receptive fields delineated on the hindhoof. E. Receptive fields delineated on the forehoof. F. Receptive fields found on the ventral shoulder. Receptive fields illustrated in C, D, E, and F were found at the corresponding penetration sites in A. Receptive field 12b in Fig. 5F was bilateral.
S.L. CRANER AND R.H. RAY
48 they point away from, the anterior suprasylvian sulcus. According to Burton and Robinson (’81),it is possible, however, to interpret the cat SII as having a striplike organization, similar to the map seen in the monkey, in which the limbs follow oblique anterior to posterior “nested strips” across SII (Burton and Robinson, ’81). This “dermatomal-strip” organization is similar to that found in our study of the pig SII cortex. The digits and limbs do not point toward or away from the suprasylvian sulcus, but are represented in anterior t o posterior nested strips across SII. The trunk representation seems to curve posterolaterally to the digit and limb representations, thus giving the pig SII what can be considered to be an inverted organization. Like the pig, the sheep and llama are members of the Arteriodactyla order. The llama, a member of the suborder Tylopoda, has an inverted SII (Welker et al., ’76),similar to that of the pig, a member of the suborder Suiformes. Sheep, however, members of the suborder Ruminantia, demonstrate an erect SII region (Johnson et al., ’74). These findings indicate that dissimilar cortical plans of organization can exist in mammals of the same order. In contrast, the SII representations of the sheep and llama may need to be reexamined to determine whether a dermatomal-like organization is present, thereby resolving the disparate portrayals of SII organization. It has been suggested that SI may be a cortical region primarily devoted to a complex representation of specialized areas specific to each species’ behavioral adaptations, whereas SII may provide a more complete generalized representation of the entire body surface. Evidence from our studies supports this idea. The SII trunk and hindlimb representations were larger, better defined, and had a more regular progression of receptive fields than the corresponding representations in SI. SII also had a more generalized input from the face, primarily from the lower cheeks, chin, jaw, and ear. Few receptive fields in the mouth were found and no specialized representation of the rostrum was present in SII. By contrast, SI contained very elaborate rostrum and face representations that received input from the entire face and head, including the mouth, lips, and tongue. The SI trunk and hindlimb representations were poorly developed and there was a great deal of overlap in the forehoof, foreleg, and shoulder representations. These facts support the idea that SII provides a more generalized representation of the entire body surface, whereas SI is a more specialized body representation reflecting the behavioral adaptation of the animal.
ACKNOWLEDGMENTS We would like to thank Alan Branigan and the East Carolina University Center for Health Sciences Communications for their help with the illustrations. Partial support of this work was provided by Sigma Xi, the Scientific Research Society.
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