Current Biology 24, 109–115, January 6, 2014 ª2014 Elsevier Ltd All rights reserved

http://dx.doi.org/10.1016/j.cub.2013.11.049

Report The Representation of Social Facial Touch in Rat Barrel Cortex Evgeny Bobrov,1,2 Jason Wolfe,1 Rajnish P. Rao,1 and Michael Brecht1,* 1Bernstein Center for Computational Neuroscience, Humboldt University of Berlin, Philippstrasse 13, Haus 6, 10115 Berlin, Germany 2Berlin School of Mind and Brain, Humboldt University of Berlin, Unter den Linden 6, 10099 Berlin, Germany

Summary Controlled presentation of stimuli to anesthetized [1] or awake [2] animals suggested that neurons in sensory cortices respond to elementary features [3, 4], but we know little about neuronal responses evoked by social interactions. Here we investigate processing in the barrel cortex of rats engaging in social facial touch [5, 6]. Sensory stimulation by conspecifics differs from classic whisker stimuli such as deflections, contact poles [7, 8], or textures [9, 10]. A large fraction of barrel cortex neurons responded to facial touch. Social touch responses peaked when animals aligned their faces and contacted each other by multiple whiskers with small, irregular whisker movements. Object touch was associated with larger, more regular whisker movements, and object responses were weaker than social responses. Whisker trimming abolished responses. During social touch, neurons in males increased their firing on average by 44%, while neurons in females increased their firing by only 19%. In females, socially evoked and ongoing firing rates were more than 1.5-fold higher in nonestrus than in estrus. Barrel cortex represented socially different contacts by distinct firing rates, and the variation of activity with sex and sexual status could contribute to the generation of gender-specific neural constructs of conspecifics. Results Social facial touch is a prominent component of social interactions in rodents that strongly engages their whiskers. Here, we investigate its neuronal correlates in the whisker representation of primary somatosensory cortex (barrel cortex). To cope with the complexity of social touch, we combine neuronal recordings with high-speed videography and whisker removal and recompute neuronal data from interactions in head-centered space. We ask whether and how barrel cortex neurons respond to social touch. Barrel Cortex Responses to Social Touch Rats interacted with one or two stimulus animals across a gap (Figure 1A) allowing spontaneous approach and mutual touch, experimentally controlled choice of interaction partners, and direct comparison of responses to different animals. Interactions started with whisker overlap and typically also included nose touch. Head contours, whisker positions, and motion parameters were determined using high-speed

*Correspondence: [email protected]

videography (Figure 1B). We placed electrolytic lesions and determined histologically the laminar position of recorded cells. A layer 5B cell (Figure 1C) showed pronounced changes in neuronal firing during interactions (Figures 1D and 1E). With decreasing nose-to-nose distance, whisking decreased in amplitude and became more irregular (Figure 1F) [5]. We used standard clustering techniques to separate multichannel tetrode signals into single- and multiple-unit activity (Figures S1A–S1C available online) and classified single units by spike shape into regular-spiking, putatively excitatory, and fastspiking, putatively inhibitory neurons (Figures S1D and S1E). We recorded from 331 single and 247 multiple units from the barrel cortex of eight female and six male rats during and around 3,571 facial interactions. We restrict our report to data from regular-spiking neurons (with exception of Figures 2G and 2H as detailed there) because recordings in fast-spiking neurons were fewer in number and were distributed unevenly across animals and sexes. The histological assignment of recorded units to layers revealed pronounced laminar differences in responses to social touch (Figure S2). Layer 5B was not only the most active, but also the layer most strongly modulated by social interactions (Figure S2C). Across the population, 40% of neurons (128 out of 320 in animals with untrimmed whiskers) showed significant rate changes. The huge proportion of neurons changing firing rates indicates that barrel cortex is strongly and reproducibly engaged by social touch. Social Touch versus Object Touch and the Effects of Whisker Trimming To assess whether and how social touch differs from object touch, we compared interactions of rats with conspecifics with interactions with objects (Figure 2A). Social touch was associated with small-amplitude, irregular whisker movements, whereas object touch led to larger-amplitude, more regular whisking (Figure 2B), and this pattern was observed in numerous interactions (Figure 2C). Despite the smalleramplitude whisking during social touch, we found that social interactions evoked stronger responses in barrel cortex (Figures 2D and 2E). To investigate how sensory alterations affect social responses, we trimmed either the subject or stimulus rat’s whiskers. When the subject rat was trimmed during an interaction experiment (Figure 2F), responses were diminished (Figure 2G). This loss of responses was seen for all but one unit (Figure 2H). Across-cell comparisons also indicated that whisker trimming abolished responses (11 single units from trimmed animals). In contrast, trimming of the stimulus animal did not influence responses. The mean firing rate during interactions with trimmed stimulus animals was 1.36 Hz (median 0.28 Hz) and was only slightly higher for the same cells during touch of untrimmed stimuli (mean 1.45 Hz, median 0.27 Hz; p = 0.600, n = 41). Facial Proximity Determines Responses To average across interactions in a meaningful way, we computed head-centered interaction and firing maps in a subset of data (Figure 3). To this end, we rotated and replotted the positions of the nose of the stimulus rat and the

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Figure 1. Barrel Cortex Responses to Social Facial Touch (A) Setup. Tetrode recordings were obtained in the barrel cortex of the subject rat. (B) Schematic of whisker motion measurements. (C) Cytochrome oxidase stain of a coronal barrel cortex section. Black triangles, lesions (spaced z500 mm apart); dashed line, tetrode track; white triangle, recording site (cell shown in D–F). (D) Rasterplot of the response of a layer 5B regular-spiking neuron by interactions. The red line indicates the time of first whisker overlap. (E) Peristimulus time histogram of responses shown in (D). (F) Whisker motion and nose-to-nose distance in an interaction (underlaid gray in D). See also Figures S1 and S2.

spikes evoked at the corresponding positions to a headcentered representation relative to the subject animal (see the Experimental Procedures). Figure 3A displays nose position traces during interactions and the spikes fired of a single unit (for which whisker D3 was the principal whisker). Rats spent most time in nose contact, as shown in the occupancy map in Figure 3B. Neuronal responses varied with the relative position of the stimulus rat’s nose (Figure 3C) and peaked at positions of nose contact. The population data shown in Figures 3D–3F indicate similar conclusions. Thus, we find that most time was spent in nose contact (Figure 3E) and that barrel cortex activation was maximal in these periods (Figure 3F). These observations suggest that either rats position themselves such that interactions result in maximal barrel cortex activity or that barrel cortex units acquired a tuning that matches the most common interaction configuration.

Sex Determines Social Responses We found that responses to social touch varied with the sex of the recorded animal. As shown in Figure 4A for a neuronal recording from a female rat, this cell showed a clear response increase during interactions with males, while levels of activity in and around interactions with females were lower and responses did not increase at interaction onset. A neuron recorded from a male (Figure 4B), however, showed strong and similar responses to interactions with both sexes. On the population level, a similar picture emerged. Regular-spiking neurons from females (Figures 4C and 4E) showed smaller response modulations than neurons from males (Figure 4D). Overall, neurons from females increased their mean firing rate during interactions with both males and females from baseline (3.14 Hz) by only 19% to 3.73 Hz and were close to the unity line in the baseline versus interaction firing rate scatterplots (Figures 4C and 4E). The corresponding median firing rate increased by only 7% from 1.66 Hz to 1.77 Hz. At the same time, neurons from males (Figure 4D) showed a marked 44% mean firing rate increase from baseline (2.33 Hz) to 3.35 Hz, and the median firing rate increased by 22% from 0.93 Hz to 1.13 Hz. Responses in Females Vary with the Estrus Cycle To assess the effects of estrus cycle on responses in females, we divided female responses into estrus and nonestrus subsets. To this end, we determined phases of estrus cycle in female rats using vaginal smears. Both mean baseline (3.46 Hz in nonestrus versus 1.77 Hz in estrus) and mean evoked (3.76 Hz in nonestrus versus 2.24 Hz in estrus) firing rates varied with estrus cycle (Figures 4C and 4E). The corresponding median values were also much higher in nonestrus than in estrus for both baseline (2.06 versus 0.59 Hz) and evoked (1.98 Hz versus 0.47 Hz) firing rates. Figures 4C–4E show firing rate differences, but do not reveal the stimulus selectivity very well. Stimulus selectivity is better

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Figure 2. Social Touch, Object Touch, and the Effects of Whisker Trimming (A) Schematic of social touch (top right) or object touch (bottom right). (B) Whisking traces and nose distances for social touch (top) and object touch (bottom). Whisking amplitudes are smaller and much less regular during social interactions. (C) Whisking power is higher in object touch (n = 20 interactions) than in social touch (n = 200). (D) Peristimulus time histogram of a single unit for social touch (top) and object touch (bottom). The red line indicates the time of first whisker contact. (E) Firing rates during social touch are higher than during object interactions. The plot shows a randomly drawn subset of one third of the data, while statistics is reported for the whole population. The example unit shown in (D) is highlighted by green arrows. (F) Schematic of recordings from a subject rat before and after whisker trimming. (G) Peristimulus time histogram of an example multiple unit recorded before (top) and after (bottom) whisker trimming. (H) Firing rates of barrel cortex units decreased after whisker trimming. Both single- and multiple-unit responses were included, and a fastspiking neuron firing at w40 Hz is not shown. The example unit shown in (G) is highlighted by green arrows.

captured by response indices (computed as described in the Experimental Procedures), where +1 indicates maximal excitation, 21 indicates maximal inhibition, and 0 indicates no change of activity. Response indices for interactions of females in and out of estrus and for interactions of males are shown in Figure 4F. In females in nonestrus, responses to males and females were similar and on average weakly excitatory. In estrus, however, responses to males did not change much, whereas responses to females became inhibitory. It should be noted that this inhibitory effect seen in Figure 4F was evident mainly in cells with very low firing rates. In males, responses to males and females were similar and strongly excitatory. As shown in Figure 4F, many of these differences were highly significant, enforcing the view that subject sex, gender of the interaction partner, and estrus cycle are major determinants of responses in barrel cortex.

Whisker Motion Parameters Do Not Predict Social Responses We wondered whether differences in neuronal responses were due to differential whisking behavior. We therefore tracked whiskers in 200 interactions involving 33 pairs of interacting animals and analyzed the relation of whisking parameters (whisking power and set angle of whisking movements) and neuronal responses in this data subset (same as specified in Figures 3D–3F). For the male and female example cells (Figures 4A and 4B), neither subject rat (Figures S3A–S3D) nor stimulus rat (Figures S3E–S3H) whisking parameters were significantly correlated with response indices. Figure S3 shows that the sex-dependent responses reported in Figure 4A come about without corresponding whisking differences. Similar observations were made at the population level, where neuronal responses were only very weakly or not at all correlated to subject rat whisking (Figures S4A–S4D) or stimulus rat whisking (Figures S4E–S4H). Discussion Strong Tactile Barrel Cortex Responses to Social Touch that Vary with Cortical Layers A large fraction (40%) of barrel cortex neurons changed significantly in their activity during social touch. This measure of social barrel cortex activation is a lower boundary estimate, because we collected a limited number of interactions per cell and the freely interacting animals were not experimentally forced to engage the principal whisker of the recorded

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Figure 3. Head-Centered Interaction and Firing Maps Reveal that Facial Proximity Drives Responses to Social Touch The positions of subject and stimulus rat are rotated to give a representation centered on the nose of the subject rat. (A) Stimulus rat nose positions during interactions (gray dots) and the spikes fired (red dots) relative to the subject rat head contour (black). (B) Occupancy map showing the summed positions of the stimulus rat nose relative to the subject rat during interactions. (C) Firing rate map (firing normalized by occupancy time). (D–F) Population data recorded in both hemispheres, with conventions as in (A)–(C). For recordings from the left hemisphere, the image was reflected along the midline. Since activity in the resulting firing map was not restricted to the left contralateral hemifield, one can conclude that the contributing units had bilateral response fields. Data refer to 200 interactions and 52 regular-spiking units.

neurons. Strong barrel cortex responses to active touch have also been observed by voltage-sensitive dye imaging in awake animals [11, 12]. According to our quantification, responses to social touch were stronger than responses evoked by object touch. Trimming the subject animals abolished responses in line with the representation of whisker inputs in barrel cortex [13]. Since most tactile stimulation in social touch seems to result from whisker-to-whisker contact [5], it is surprising that trimming of stimulus animals had no significant effect on responses. This observation might indicate that adaptive alterations in touch maintain responses to whiskertrimmed animals. Specifically, we wonder whether rats—in the absence of stimulus whiskers—bring their whiskers onto the snout of the whisker-trimmed stimulus animals. Such a contact pattern might be expected if rats try to contact the conspecific with as many whiskers as possible, as has been described for obstacle contacts in the framework of the minimum-impingement strategy [14] by Prescott and colleagues. Our findings that the infragranular layers and in particular layer 5B discharge most strongly during social touch are similar to observations on layer-specific activation of barrel cortex during whisking [15] or in an aperture-discrimination task [16].

Facial Proximity Drives Responses Head-centered interaction maps revealed a strong increase of barrel cortex activity with facial proximity. The rats’ noses were aligned in facial interactions, bringing into contact both macrovibrissae and anterior snout microvibrissae, an approach behavior resembling object contacts [17]. The huge cortical representations of macro- and snout microvibrissae [18] responded strongly in facial touch. The correspondence of firing rate and occupancy maps suggests that rats align facially such that they maximally activate their barrel cortices. We have shown previously that whisker trimming disrupts facial alignment [5]. The reduction in activity in barrel cortex in response to social facial touch in whisker-trimmed animals may account for the reduced expression of the behavior of facial touch as a consequence of whisker trimming. Object Touch, Social Touch, and Neural Responses The differential whisking observed in object and social facial interactions highlights the behavioral flexibility of rodent active touch [19]. We note, however, that it is unclear at this stage whether such differences in whisker movements account for the weaker neural responses to object touch. In social facial touch, whisking parameters were not or at the most very weakly

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Figure 4. Sex Dependence of Barrel Cortex Responses to Social Facial Touch Responses during interactions with males are depicted in blue and those with females in red. (A) Peristimulus time histogram of single-unit activity from female barrel cortex reveals weak modulation, particularly during interactions with females. (B) Single-unit recording from male barrel cortex. Note the stronger and similar responses in interactions with both sexes. (legend continued on next page)

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correlated to neuronal responses (Figures S3 and S4). Instead, we observed a wide range of neuronal responses for the same whisking parameters. The weak correlation of whisking to spikes [20] and membrane potential [21] might contribute to the lack of correlation between responses and subject whisking. Still, the lack of a correlation between responses and stimulus rat whisking power (Figure S4) remains a puzzle because facial touch leads to intense whisker contacts [5] and barrel cortex responses were shown to strongly increase with stimulus velocity [22]. While neither subject nor stimulus rat whisking parameters did predict neuronal responses, this observation does not rule out the possibility that subtle tactile variations in social touch escaped our quantification and led to the differential neural responses in social touch. Sex and Estrus Cycle Are Major Determinants of Barrel Cortex Responses Sex is a major biological determinant of social interactions, and we demonstrate marked sex differences in cortical responses. The sheer magnitude of the sex and estrus differences (a 2.3 times larger response modulation in males than in females; more than 1.5 times higher firing in females in nonestrus compared to estrus) is impressive and much larger than the effect of attentional modulation in early visual areas [23]. Minor sex differences in barrel cortex organization have been described [24], but the exact origin and neural substrate of sex differences in responsiveness is not yet clear. It seems likely, but not certain, that the sex-specific responses observed here are different from the barrel cortex response properties studied so far. Conventional sensory selectivities, such as angular or velocity tuning, represent the results of sensory analysis about mechanical properties. In contrast, the sex differences that we observed probably result from attentional effects and/or multisensory integration. Conclusions The rich social information available in barrel cortex responses differs profoundly from the dorsal hippocampus of the rat, where only very weak and nondiscriminative social responses were observed [25]. Responses observed here varied with animal sex, gender of the interaction partner, and sexual status. Our findings make us wonder whether barrel cortex assigns social attributes to tactile inputs and hence is involved in the generation of social neural constructs (‘‘these tactile contacts refer to male/female,’’ etc.). The idea that somatosensory cortex represents social meaning in addition to pure stimulus mechanics is supported by findings from humans [26]. Hence, the representation in somatosensory cortex appears less ‘‘primal’’ and more ‘‘high-level’’ than envisioned by early theories of sensory processing [27]. This insight calls for further investigation of cortical activity in behaviorally and biologically meaningful contexts. Experimental Procedures For details, please see the Supplemental Experimental Procedures. Extracellular recordings with tetrodes were performed in the posteromedial barrel subfield of primary somatosensory cortex of eight female and six male adult

Wistar rats. Experimental procedures complied with German guidelines on animal welfare (permit G0259/09). Social interactions were videotaped under infrared illumination. Three behavioral events were detected: time of first whisker overlap; time of nose-to-nose contact, where applicable; and end of whisker overlap. A variety of objects of different materials were also presented. Only recordings with at least three interactions with a certain stimulus animal or object were included in the analysis. In a subset of experiments, whiskers were trimmed. For trimmed animals, interaction onsets and offsets were defined as the estimated times of whisker overlap, if intact whiskers had been present. Rats were implanted with eight movable tetrodes over the barrel cortex, in the right hemisphere for 12 of 14 animals. Spikes were sorted offline using their amplitude and spike shape, and the resulting classification was refined manually. Receptive fields were determined by deflecting single or multiple whiskers with a handheld rod and listening to neuronal responses. Nearly all receptive fields were within the macrovibrissae array. Electrolytic lesions along tetrode tracks were used to reconstruct recording locations and layers. Before experiments, rat whiskers (typically C2) were tagged. Periods of social interactions were recorded using a high-speed camera (250 Hz). Whisker tracking was performed for a subset of 200 interactions. We also analyzed relative head positions during interactions and neuronal responses in a space centered on the subject rat head. The respective head direction vector of the stimulus rat was rotated correspondingly. Occupancy and firing maps were calculated by discretizing space into bins, summing occupancy or firing in this bin over time, smoothing the data, and pooling over days. Firing rate modulation during social interactions with either sex was quantified by comparing the average firing rate during all interactions with that sex with a matched-length baseline period outside of interactions. Response indices are defined as follows: response index = (r 2 n) / (r + n), where r and n are the interaction and baseline firing rates, respectively. Estrus was determined from vaginal smears. Differences between groups were tested with Wilcoxon signed-rank test for paired data and the Mann-Whitney U test for unpaired data. One, two, and three asterisks indicate significance levels of 0.05, 0.01, and 0.001, respectively. Supplemental Information Supplemental Information includes Supplemental Experimental Procedures and four figures and can be found with this article online at http://dx.doi.org/ 10.1016/j.cub.2013.11.049. Acknowledgments This work was supported by Humboldt University of Berlin, the Bernstein Center for Computational Neuroscience Berlin, the German Federal Ministry of Education and Research (BMBF, Fo¨rderkennzeichen 01GQ1001A), Neurocure, a Berlin School of Mind and Brain scholarship to E.B., and a European Research Council grant to M.B. We thank Brigitte Geue, Andreea Neukirchner, Undine Schneeweiß, and Juliane Steger for outstanding technical assistance and Andrea Burgalossi, Guy Doron, Christian Ebbesen, Constanze Lenschow, and Moritz von Heimendahl for comments. The latter also contributed to the analysis software. We also thank Viktor Bahr for implementing the head-centered analysis, as well as Tiziano D’Albis and Falk Mielke for help with tracking and software development. Received: April 22, 2013 Revised: October 29, 2013 Accepted: November 26, 2013 Published: December 19, 2013 References 1. Hubel, D.H., and Wiesel, T.N. (1977). Ferrier lecture. Functional architecture of macaque monkey visual cortex. Proc. R. Soc. Lond. B Biol. Sci. 198, 1–59. 2. Wurtz, R.H. (1968). Visual cortex neurons: response to stimuli during rapid eye movements. Science 162, 1148–1150.

(C) Scatterplot of single-unit activity during baseline (outside of interactions) against responses during facial interactions in female barrel cortex while subject female was in nonestrus. The example unit shown in (A) is highlighted by green arrows. (D) Same as (C) for recordings in male barrel cortex. The unit highlighted by green arrows corresponds to the one shown in (B). (E) Same as (C) for recordings while the subject female was in estrus. Note that firing rates are lower than was observed in nonestrus. (F) Population data for response indices (+1, maximal excitation; 21, maximal inhibition; 0, no change of activity in interactions). Error bars indicate the SEM. In (C)–(F), each data point corresponds to one stimulus animal. See also Figures S3 and S4.

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The representation of social facial touch in rat barrel cortex.

Controlled presentation of stimuli to anesthetized [1] or awake [2] animals suggested that neurons in sensory cortices respond to elementary features ...
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