The cellular mechanisms of emotional contagion are unknown. We investigated tickle contagion and the underlying neuronal representations in playful rats. We recorded trunk somatosensory cortex activity of observer rats while they received tickling and audiovisual playback of tickling footage and while they witnessed tickling of demonstrator rats. Observers vocalized and showed "Freudensprünge" ("joy jumps") during witnessing live tickling, while they showed little behavioral responses to playbacks. Deep layers in the trunk somatosensory neurons showed a larger correlation between direct and witnessed tickling responses compared to superficial layers. Trunk somatosensory neurons discharged upon emission of own and demonstrator's vocalizations and might drive contagious "laughter". We conclude that trunk somatosensory cortex might represent ticklishness contagion.

Whole-cell voltage recordings were made in vivo from excitatory neurons (n = 23) in layer 4 of the barrel cortex in urethane-anaesthetised rats. Their receptive fields (RFs) for a brief whisker deflection were mapped, the position of the cell soma relative to barrel borders was determined for 15 cells and dendritic and axonal arbors were reconstructed for all cells. Three classes of neurons were identified: spiny stellate cells and pyramidal cells located in barrels and pyramidal cells located in septa. Dendritic and, with some exceptions, axonal arborisations of barrel cells were mostly restricted to the borders of a column with a cross sectional area of a barrel, defining a cytoarchitectonic barrel-column. Dendrites and axons of septum cells, in contrast, mostly extended across barrel borders. The subthreshold RFs measured by evoked postsynaptic potentials (PSPs) comprised a principal whisker (PW) and several surround whiskers (SuWs) indicating that deflection of a single whisker is represented in multiple barrels and septa. Barrel cells responded with larger depolarisation to stimulation of the PW (13.7 +/- 4.6 mV (mean +/- S.D.), n = 10) than septum cells (5.7 +/- 2.4 mV, n = 5), the gradient between peak responses to PW and SuW deflection was steeper and the latency of depolarisation onset was shorter (8 +/- 1.4 ms vs. 11 +/- 2 ms). In barrel cells the response onset and the peak to SuW deflection was delayed depending on the distance to the PW thus indicating that the spatial representation of a single whisker deflection in the barrel map is dynamic and varies on the scale of milliseconds to tens of milliseconds. Septum cells responded later and with comparable latencies to PW and SuW stimulation. Spontaneous (0.053 +/- 0.12 action potentials (APs) s(-1)) and evoked APs (0.14 +/- 0.29 APs per principal whisker (PW) stimulus) were sparse. We conclude that PSPs in ensembles of barrel cells represent dynamically the deflection of a single whisker with high temporal and spatial acuity, initially by the excitation in a single PW-barrel followed by multi-barrel excitation. This presumably reflects the divergence of thalamocortical projections to different barrels. Septum cell PSPs preferably represent multiple whisker deflections, but less dynamically and with less spatial acuity.

Female mammals experience cyclical changes in sexual receptivity known as the estrus cycle. Little is known about how estrus affects the cortex, although alterations in sensation, cognition and the cyclical occurrence of epilepsy suggest brain-wide processing changes. We performed in vivo juxtacellular and whole-cell recordings in somatosensory cortex of female rats and found that the estrus cycle potently altered cortical inhibition. Fast-spiking interneurons were strongly activated with social facial touch and varied their ongoing activity with the estrus cycle and estradiol in ovariectomized females, while regular-spiking excitatory neurons did not change. In situ hybridization for estrogen receptor β (Esr2) showed co-localization with parvalbumin-positive (PV+) interneurons in deep cortical layers, mirroring the laminar distribution of our physiological findings. The fraction of neurons positive for estrogen receptor β (Esr2) and PV co-localization (Esr2+PV+) in cortical layer V was increased in proestrus. In vivo and in vitro experiments confirmed that estrogen acts locally to increase fast-spiking interneuron excitability through an estrogen-receptor-β-dependent mechanism.

Social interactions involve multi-modal signaling. Here, we study interacting rats to investigate audio-haptic coordination and multisensory integration in the auditory cortex. We find that facial touch is associated with an increased rate of ultrasonic vocalizations, which are emitted at the whisking rate (∼8 Hz) and preferentially initiated in the retraction phase of whisking. In a small subset of auditory cortex regular-spiking neurons, we observed excitatory and heterogeneous responses to ultrasonic vocalizations. Most fast-spiking neurons showed a stronger response to calls. Interestingly, facial touch-induced inhibition in the primary auditory cortex and off-responses after termination of touch were twofold stronger than responses to vocalizations. Further, touch modulated the responsiveness of auditory cortex neurons to ultrasonic vocalizations. In summary, facial touch during social interactions involves precisely orchestrated calling-whisking patterns. While ultrasonic vocalizations elicited a rather weak population response from the regular spikers, the modulation of neuronal responses by facial touch was remarkably strong.

The mammalian somatosensory cortex shows marked species-specific differences. How evolution in general and sexual selection in particular shape the somatosensory cortical body representation has not been delineated, however. Here we address this issue by a comparative analysis of genital cortex. Genitals are unique body parts in that they show sexual dimorphism, major changes in puberty and typically more pronounced species differences than other body parts (Hosken & Stockley, 2004). To study the evolution of genital cortex we flattened cortical hemispheres and assembled 104 complete body maps, revealed by cytochrome-oxidase activity in layer 4 of 8 rodent and 1 lagomorph species. In two species, we also performed antibody stainings against vesicular glutamate transporter-2, which suggested that cytochrome-oxidase maps closely mirror thalamic innervation. We consistently observed a protrusion between hindlimb and forelimb representation, which in rats (Lenschow et al., 2016) corresponds to the penis representation in males and the clitoris representation in females. Consistent with the idea that this protrusion corresponds to genital cortex, we observed a size increase of this protrusion during puberty. Species differed in external genital sexual dimorphism, but we observed a sexual monomorphism of the putative genital protrusion in all species, similar to previous observations in rats. The relative size of the putative genital protrusion varied more than 3-fold between species ranging from 0.5% of somatosensory cortex area in chipmunks to 1.7% in rats. This relative size of the genital protrusion co-varied with relative testicle size, an indicator of sperm competition and sexual selection.

The parahippocampal region is organized into different areas, with the medial entorhinal cortex (MEC), presubiculum and parasubiculum prominent in spatial memory. Here, we also describe a region at the extremity of the MEC and bordering the subicular complex, the medial-most part of the entorhinal cortex. While the subdivisions of hippocampus proper form more or less continuous cell sheets, the superficial layers of the parahippocampal region have a distinct modular architecture. We investigate the spatial distribution, laminar position, and putative connectivity of zinc-positive modules in layer 2 of the MEC of rats and relate them to the calbindin-positive patches previously described in the entorhinal cortex. We found that the zinc-positive modules are complementary to the previously described calbindin-positive patches. We also found that inputs from the presubiculum are directed toward the zinc-positive modules while the calbindin-positive patches received inputs from the parasubiculum. Notably, the dendrites of neurons from layers 3 and 5, positive for Purkinje Cell Protein 4 expression, overlap with the zinc modules. Our data thus indicate that these two complementary modular systems, the calbindin patches and zinc modules, are part of parallel information streams in the hippocampal formation.

The home is a unique location in the life of humans and animals. In rats, home presents itself as a multicompartmental space that involves integrating navigation through subspaces. Here we embedded the laboratory rat's home cage in the arena, while recording neurons in the animal's parasubiculum and medial entorhinal cortex, two brain areas encoding the animal's location and head direction. We found that head direction signals were unaffected by home cage presence or translocation. Head direction cells remain globally stable and have similar properties inside and outside the embedded home. We did not observe egocentric bearing encoding of the home cage. However, grid cells were distorted in the presence of the home cage. While they did not globally remap, single firing fields were translocated toward the home. These effects appeared to be geometrical in nature rather than a home-specific distortion and were not dependent on explicit behavioral use of the home cage during a hoarding task. Our work suggests that medial entorhinal cortex and parasubiculum do not remap after embedding the home, but local changes in grid cell activity overrepresent the embedded space location and might contribute to navigation in complex environments.NEW & NOTEWORTHY Neural findings in the field of spatial navigation come mostly from an abstract approach that separates the animal from even a minimally biological context. In this article we embed the home cage of the rat in the environment to address some of the complexities of natural navigation. We find no explicit home cage representation. While both head direction cells and grid cells remain globally stable, we find that embedded spaces locally distort grid cells.

Whole-cell voltage recordings were made in vivo in the ventral posterior medial nucleus (VPM) of the thalamus in urethane-anaesthetised young (postnatal day 16-24) rats. Receptive fields (RFs) on the whisker pad were mapped for 31 neurones, and 10 cells were recovered for morphological reconstruction of their dendritic arbors. Most VPM neurones had antagonistic subthreshold RFs that could be divided into excitatory and inhibitory whiskers. VPM cells comprised different classes, the most frequently occurring being single-whisker excitation (SWE) and multi-whisker excitation (MWE) cells. In SWE cells (36 % of VPM neurones), only principal whisker (PW) deflection evoked an EPSP and was followed by a single action potential (AP) or remained subthreshold. The depolarisation was terminated by a large, delayed IPSP. A stimulus evoked on average 0.74 +/- 0.46 APs (mean +/- S.D.) with short latency (8.1 +/- 1.0 ms) and small temporal scatter (0.31 +/- 0.23 ms dispersion of 50 % of the first APs). In MWE cells (29 % of VPM neurones), deflection of several whiskers evoked EPSPs. PW responses were either subthreshold EPSPs or consisted of an EPSP followed by one or several APs (0.96 +/- 0.99 APs per stimulus). AP responses were often associated with putative low-threshold calcium-dependent regenerative potentials and were followed by a small delayed IPSP. AP responses had a longer latency (12.3 +/- 2.6 ms) and larger temporal scatter (2.5 +/- 1.6 ms) than responses of SWE cells. MWE cells had a lower input resistance than SWE cells. The elongation of dendritic arbors along the representation fields of rows and arcs in VPM barreloids was weakly correlated with the subthreshold RF elongation along whisker rows and arcs, respectively. Evoked EPSP-AP responses exhibited a sharper directional tuning than subthreshold EPSPs, which in turn exhibited a sharper directional tuning than IPSPs. In conclusion, we document two main classes of VPM neurones. SWE cells responded with a precisely timed single AP to the deflection of the PW. In contrast, MWE cell RFs were more broadly tuned and the temporally dispersed multiple AP responses of these cells represented the degree of collective deflection of the PW and several adjacent whiskers.