A Non-canonical Feedback Circuit for Rapid Interactions between Somatosensory Cortices

Abstract

SUMMARYSensory perception depends on interactions among cortical areas. These interactions are mediated by canonical patterns of connectivity in which higher areas send feedback projections to lower areas via neurons in superficial and deep layers. Here, we probed the circuit basis of interactions among two areas critical for touch perception in mice, whisker primary (wS1) and secondary (wS2) somatosensory cortices. Neurons in layer 4 of wS2 (S2L4) formed a major feedback pathway to wS1. Feedback from wS2 to wS1 was organized somatotopically. Spikes evoked by whisker deflections occurred nearly as rapidly in wS2 as in wS1, including among putative S2L4 → S1 feedback neurons. Axons from S2L4 → S1 neurons sent stimulus orientation-specific activity to wS1. Optogenetic excitation of S2L4 neurons modulated activity across both wS2 and wS1, while inhibition of S2L4 reduced orientation tuning among wS1 neurons. Thus, a non-canonical feedback circuit, originating in layer 4 of S2, rapidly modulates early tactile processing.

Spatiotemporal properties of whisker-evoked tactile responses in the mouse secondary somatosensory cortex

“…At the population level (n = 9 mice), responses in S2 presented an overall small but significant delay in latency (+3.3 +/− 1.2 ms, Fig. 3b2,b3), consistently with recently reported electrophysiological data 8 . Although the amplitude of evoked responses was smaller in S2 than in S1 for the illustrated case ( Fig.…”

“…Each neuronal column associated with a barrel receives primarily the input coming from its corresponding whisker. Upon tactile stimulation of a given whisker, information is indeed rapidly transmitted to its corresponding barrel in S1, but also, within the next couple of milliseconds, to the secondary somatosensory cortex S2 [5][6][7][8] . The rapid activation of S2 neurons following whisker stimulation is likely to rely on the direct projections it receives from both the ventral posteromedial nucleus [9][10][11] and the posteromedial complex of the thalamus [12][13][14] .…”

“…Hence, although S2 is usually considered as a higher order area compared to S1, it seems that cortical processing of tactile information follows a parallel, rather than hierarchical, scheme in rodents. The S2 cortex is nonetheless densely interconnected with S1, in a reciprocal and topographic manner 8,[15][16][17][18][19][20][21] .…”

Unique properties of high-order thalamic inputs versus cortical inputs to primary somatosensory cortex

“…Additionally, our study provides a direct anatomical comparison of these three long-range projections. The overall laminar distributions of POm, M1, and S2 projections to barrel cortex here are consistent with previous observations of the individual projections (Kinnischtzke et al, 2014;Minamisawa et al, 2018;Ohno et al, 2012;Veinante and Deschenes, 2003;Wimmer et al, 2010). We found that these three areas differ in their infragranular targets.…”

Layer-specific sensory processing impairment in the primary somatosensory cortex after motor cortex infarction

“…Infarct volumes were calculated using ImageJ by measuring the largest area of the infarct in all 4 coronal sections, which was normalised by the ratio of ipsilesional to contralesional cortical volumes 5 to exclude the shift effect of cortex. 6 7 In vivo electrophysiological recording 8 Electrophysiological recordings were performed at postoperative day 3 (POD3) and POD14, which 9 correspond to the acute and subacute phases of the infarction, respectively (Fig. 1).…”