Neuroscience Letters, 143 (1992) 237 242 © 1992 Elsevier Scientific Publishers Ireland Ltd. All rights reserved 0304-3940/92/$ 05.00

237

NSL 08899

Thalamocortical connections of rat posterior parietal cortex H.C. Chandler a'b, V. King d, J.g. C o r w i n e a n d R.L. R e e p b'c Departments of"Neurological Surgery, hNeuroscience and ~Physiological Sciences, University of Florida, Gainesville, FL ( USA ), JDepartmenl ~l' Psychology, University of Wisconsin, Madison, WI (USA) and 'Department of Psychology, Northern Illinois" University, De Kalb, IL ( USA ) (Received 2 January 1992; Revised version received 8 May 1992; Accepted 28 May 1992)

K¢v wordsv Posterior parietal cortex; Thalamocortical connection: Rat cortex; Attention The neuronal connections of rat posterior parietal cortex (PPC) have been examined using retrograde fluorescent axonal tracers. We have tbund that PPC receives thalamic input predominantly from the lateral posterior and lateral dorsal nuclei, and not from the ventrobasal nucleus, which projects to the rostrally adjacent hindlimb cortex, or from the dorsal lateral geniculate nucleus, which projects to the caudally adjacent visual association area. PPC has reciprocal corticocortical connections with medial agranular cortex and orbital cortex: together, these three cortical areas may function as a network for directed attention in rats.

The existence of a posterior parietal association cortex (PPC) in rodents was first suggested by Krieg [5] on cytoarchitectural grounds, apparently in analogy to Brodmann's area 7 of primates. Previous work has demonstrated that the rat PPC is involved in spatial navigation tasks [4] and is one of three cortical areas in which unilateral lesions result in contralateral multimodal neglect [1]; the other two areas are medial agranular cortex (AGm) [3] and ventrolateral orbital cortex (VLO) [2]. This implicates each of these areas as having a role in spatial orientation and directed attention. Rat PPC as defined by these behavioral studies lies approximately 4~6 mm posterior to bregma and 2 6 mm lateral to the midline [4]. Thus, PPC is bordered rostrally by the hindlimb area (HL) of somatic sensorimotor cortex, laterally by area Parl of somatic sensorimotor cortex, medially by the agranular portion of retrosplenial cortex, and caudally and laterally by area OC2 of visual association cortex. On the basis ofcytoarchitecture, PPC is easily distinguishable from area H L by its reduced granular layer IV and the lack of cell-sparse zones above and below layer V. However, we have not found it possible to separate PPC from area OC2 on cytoarchitectural grounds. In contrast to previous reports [4, 6], we find no compressed layer II in PPC and no consistent differences between PPC and OC2 in laminar widths or densities. Therefore, it is necessary to examine patterns of conCorrespondenee: R.L. Reep, Department of Physiological Sciences, J144 JHMHC, University of Florida, Gainesville, FL 32610, USA.

nections in order to determine if PPC is an autonomous area. Kolb and Walkey [4] demonstrated that the putative rat PPC receives thalamic input from the lateral posterior nucleus. However, it was not clear from this study whether the connections of PPC differ from those of surrounding cortical areas. In the present study we used axonal tracing techniques to determine whether the pattern of thalamic input to PPC is distinct from those of neighboring cortical areas, and to discover the extent to which PPC is interconnected with the other two cortical areas involved in spatial orientation and directed attention, A G m and VLO. Eighteen rats (hooded and albino) weighing 250~100 g were used. In some cases a single cortical injection of the fluorescent retrograde tracer Fluoro-Gold (FG) or Fast Blue (FB) was made, whereas in other cases FG and FB were injected in neighboring cortical areas. All injections were made using a Picospritzer (General Valve Corp.) for controlled nitrogen pressure injections (1 2 pulses, 20-40 psi, 3-10 ms) through micropipettes having tip diameters of 20 30/am. After survival times of 4 5 days, animals were perfused and tissue processed as described previously [7]. One series of spaced coronal sections was stained with Cresyl violet and used for cytoarchitectural orientation. Traced drawings of the boundaries of thalamic nuclei were made using a macroprojector. Identification of fluorescent labeled neurons was done through the microscope, using a second series of unstained sections adjacent to the first. The locations of labeled cells were then plotted on the tracings, with features such as

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Fig. 1. Thalamic labeling plotted on representative coronal tracings, resulting from retrograde transport of Fluoro-Gold from a cortical injection centered in posterior parietal cortex• HL

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Fig. 2. Thalamic labeling plotted on representative coronal tracings, resulting from retrograde transport of Fluoro-Gold from a cortical injection centered in hindlimb sensorimotor cortex.

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Fig. 3. Thalamic labeling plotted on representative coronal tracings, resulting from retrograde transport of Fast Blue from PPC (small dots) and of Fluoro-Gold from retrosplenial cortex (large dots).

blood vessels being used as points of reference. In the illustrations below, each dot represents 1-3 labeled neurons. The four cases presented below were chosen for discussion because they illustrate the major points to be made concerning thalamic labeling patterns. Similar patterns were found in the other fourteen cases. Terminology for cortical areas follows that of Zilles [11]; the terms Fr2 and A G m are used interchangeably, as are Frl and AGI. In case PPC 167 the F G injections site (Fig. 1A) is centered in PPC above and slightly lateral to the cingulum bundle, caudal to area H L (as identified cytoarchitecturally). Medially, the injection encroaches on FR1 rostrally, as evidenced by the presence of labeled neurons in the ventrolateral (VL) nucleus of the thalamus (Fig. I B). The injection also affects retrosplenial cortex caudally, as indicated by a few labeled cells in the anterodorsal (AD) nucleus. Many labeled neurons are

found in the laterodorsal (LD) and lateroposterior (LP) nuclei (Fig. 1C,D). No labeling was seen in the ventrobasal complex (VB) or lateral geniculate nucleus (DLG). In case A G m 20 the F G injection site (Fig. 2A) is centered in area H L and encroaches on PPC caudally. Thalamic labeling is concentrated in the far lateral hindlimb portion of VB and in LD and LR but labeled cells are also seen in several other nuclei (Fig. 2B D ) . The concentration of labeling in caudal dorsomedial LD ( L D D M ) is reminiscent of the pattern reported by Kolb and Walkey [4] after large lesions or injections of True Blue in PPC (see their Fig. 2). In case PPC 177 two injections were made. A medial F G injection (Fig. 3A) was entirely confined to retrosplenial cortex, and produced concentrated labeling in the anterodorsal, anteroventral and anteromedial thalamic nuclei (AD, AV and AM), and moderate labeling in LD and LP (Fig. 3B-D). A more laterally placed FB injection was centered in PPCjust lateral to the cingulum

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Fig. 4. Thalamic labeling plotted on representative coronal tracings, resulting from retrograde transport of Fast Blue from area OC2 (small dots) and of Fluoro-Gold from retrosplenial cortex (large dots).

bundle (Fig. 3A). Thalamic labeling resulting from this injection was seen primarily in LD, LP and the posterior nucleus, PO (Fig. 3B-D). The labeled cells seen in LD and LP after these two injections were intermingled except that rostral LD contained only FB- labeled cells resulting from the injection in PPC. In case PPC 149 two injections were also made. A medial FG injection (Fig. 4A) involved the retrosplenial cortex (RS) and produced labeled neurons in the anterior thalamic nuclei, LD, LP and the caudal portion of the central lateral (CL) nucleus (Fig. 4B-D). A more lateral FB injection was located in area OC2M, with some encroachment on the underlying white matter (Fig. 4A). Thalamic labeling was focused in LD, LP, PO and DLG (Fig. 4B-D). Injections rostral to PPC which involve area HL (such as case AGm 20 above) result in labeling in VB, as do injections in area Parl lateral to PPC (not illustrated). However, VB labeling is not seen with injections placed in PPC just caudal to area HL, in RS medial to PPC, or in OC2 caudal to PPC. Anterior thalamic nuclei are labeled when injections involve area RS, but not when injections involve the other cortical locations studied. La-

beling of DLG is seen when injections involve area OC2 or OC1 (not illustrated). Some labeling of LD and LP/ PO is found in almost all cases. However, injections confined to PPC produce thalamic labeling that is densest in and virtually limited to these two nuclei, and no labeling is seen in the anterior nuclei, VB or DLG. The corticocortical connections of PPC involve primarily AGm (area Fr2 of ZiUes [11]) and orbital cortex. As illustrated in Fig. 5, an mjection of retrograde fluorescent tracer in any one of these three areas produces labeled cells in the other two. Reciprocal connections between AGm and orbital cortex were described previously [7-10] and Kotb and Walkey [4] noted input from AGm to PPC. Caudal AGm and orbital cortex have reciprocal connections with area OC2 as well as PPC [6-8, 10]. The interconnectivity among PPC, AGm and orbital cortex suggests that they may function as a cortical network for spatial orientation and directed attention. We conclude that PPC may be distinguished from other cortical areas on the basis of thatamic labehng limited to LD and LP. PPC defined on this basis is considerably more limited in extent than suggested by Kolb and Walkey [4], extending approximately 3-4 mm caudal to

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Fig. 5. Three cases representing interconnections among PPC. medial agranular cortex and orbital cortex. In case PPC 177 an injection of Fast Blue was made in PPC (see also Fig. 3). In case VLO 159 and injection of Fast Blue was centered in the ventrolateral orbital area. In case AGm 29 an injection of Fluoro-Gold was located in medial agranular cortex.

clear a n d r e p l i c a b l e , b u t m a y n o t c o r r e s p o n d to f u n c t i o n -

lege o f V e t e r i n a r y M e d i c i n e a n d by G r a n t L E Q S F - R D -

ally d e f i n e d p a r c e l l a t i o n s . F o r i n s t a n c e , it r e m a i n s to be

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d e t e r m i n e d w h e t h e r lesions r e s t r i c t e d to P P C as d e f i n e d a n a t o m i c a l l y w o u l d result in s i m i l a r b e h a v i o r a l deficits as t h o s e r e s u l t i n g f r o m the l a r g e r lesions m a d e p r e v i ously, w h i c h h a v e i n c l u d e d a r e a O C 2 . O n the o t h e r h a n d , it m a y be t h a t P P C a n d a r e a O C 2 s h a r e f u n c t i o n a l a t t r i b utes as well as c o r t i c o c o r t i c a l c o n n e c t i o n s w i t h A G m a n d orbital cortex. We t h a n k H e i d i W e a r n e for d r a w i n g t h e figures. T h i s r e s e a r c h was s u p p o r t e d by the U n i v e r s i t y o f F l o r i d a C o l -

1 Chandler, H.C., Reep, R.L., King, V. and Corwin, J.V., Posterior parietal cortex in rats: behavioral attributes and thalamic and cortical connections, Soc. Neurosci. Abstr., 17 ( 1991 ) 1585. 2 King, V., Corwin, J.V. and Reep, R.L., Production and characterization of neglect in rats with unilateral lesions of ventrolateral orbital cortex, Exp. Neurol., 105 (1989) 287 299. 3 King, V. and Corwin, J.V., Neglect following unilateral ablation of the caudal but not the rostral portion of medial agranular cortex of the rat and the therapeutic effect of apomorphine, Behav. Brain Res.,37(1990) 169 184.

242 4 Kolb, B. and Walkey, J., Behavioral and anatomical studies of the posterior patietal cortex in the rat, Behav. Brain Res., 23 (1987) 127-145. 5 Krieg, W.J.S., Connections of the cerebral cortex: I. The albino rat. B. Structure of the cortical areas, J. Comp. Neurol., 84 (1946) 277~ 323. 6 Miller, M.W. and Vogt, B.A., Direct connections of rat visual cortex with sensory, motor, and association cortices, J. Comp. Neurol., 226 (1984) 184-202. 7 Reep, R.L., Goodwin, G.S. and Corwin, J.V., Topographic organization in the corticocortical connections of medial agranular cortex in rats, J. Comp. Neurol., 294 (1990) 262-280.

8 Reep, R.L., Wallach, A., King, V. and Corwin, J.V., Patterns of connectivity in rat orbital cortex, Soc. Neurosci. Abstr,, 15 (1989) 283. 9 Reep, R.L., Corwin, J.V., Hashimoto, A. and Watson, R.T., Efferent connections of the rostral portion of medial agranular cortex in rats, Brain Res. Bull,, 19 (1987) 203-.221. 10 Reep, R.L., Corwin, J.V., Hashimoto, A. and Watson, R.F., Afferent connections of medial precentral cortex in the rat, Neurosci. Lett., 44 (1984) 247 252. 11 Zilles, K., The Cortex of the Rat, Springer, Berlin, 1985.