Cortical and thalamic contributions to response dynamics across layers of the primary somatosensory cortex during tactile discrimination

Abstract

Pais-Vieira M, Kunicki C, Tseng PH, Martin J, Lebedev M, Nicolelis MA. Cortical and thalamic contributions to response dynamics across layers of the primary somatosensory cortex during tactile discrimination. J Neurophysiol 114: 1652-1676, 2015. First published July 15, 2015 doi:10.1152/jn.00108.2015.-Tactile information processing in the rodent primary somatosensory cortex (S1) is layer specific and involves modulations from both thalamocortical and cortico-cortical loops. However, the extent to which these loops influence the dynamics of the primary somatosensory cortex while animals execute tactile discrimination remains largely unknown. Here, we describe neural dynamics of S1 layers across the multiple epochs defining a tactile discrimination task. We observed that neuronal ensembles within different layers of the S1 cortex exhibited significantly distinct neurophysiological properties, which constantly changed across the behavioral states that defined a tactile discrimination. Neural dynamics present in supragranular and granular layers generally matched the patterns observed in the ventral posterior medial nucleus of the thalamus (VPM), whereas the neural dynamics recorded from infragranular layers generally matched the patterns from the posterior nucleus of the thalamus (POM). Selective inactivation of contralateral S1 specifically switched infragranular neural dynamics from POM-like to those resembling VPM neurons. Meanwhile, ipsilateral M1 inactivation profoundly modulated the firing suppression observed in infragranular layers. This latter effect was counterbalanced by contralateral S1 block. Tactile stimulus encoding was layer specific and selectively affected by M1 or contralateral S1 inactivation. Lastly, causal information transfer occurred between all neurons in all S1 layers but was maximal from infragranular to the granular layer. These results suggest that tactile information processing in the S1 of awake behaving rodents is layer specific and state dependent and that its dynamics depend on the asynchronous convergence of modulations originating from ipsilateral M1 and contralateral S1.

Neuronal Assemblies Evidence Distributed Interactions within a Tactile Discrimination Task in Rats

“…To reduce discrepancies, we only averaged neurons of similar profile (increased, decreased, or both). Figure 4 shows the MFR of neurons presenting both increased and decreased responses (named multiphasic units), the most likely type of modulation in the cortical layer from which we recorded (Pais-Vieira et al, 2015 ). All cortical areas modulate their MFR: neuronal activity peaked in the four brain regions upon vibrissae stimulation, soon before rats reach the NP, similarly to previous findings (Pais-Vieira et al, 2013 ).…”

“…This task was originally proposed by Krupa et al ( 2001 ) and animal behavior was further studied in subsequent works (Krupa et al, 2004 ; Pantoja et al, 2007 ; Wiest et al, 2010 ; Vasconcelos et al, 2011 ; Pais-Vieira et al, 2015 ). The behavioral apparatus design results in stereotypical animal trajectories over the course of the trial, with whiskers sampling the aperture for a few hundred milliseconds.…”

“…For each trial, starting at t = −4 s and at every 350 ms time window (50 ms time step), the feature vector was determined by concatenating the mean firing rate of neurons from the given cortical region in seven consecutive 50 ms windows. Parameters were chosen based on Pantoja et al ( 2007 ), Wiest et al ( 2010 ), Vasconcelos et al ( 2011 ), and Pais-Vieira et al ( 2015 ) and analyses were robust to minor variations on this choice. The label of each feature vector was either “0” (left side reward) or “1” (right side reward).…”

Anti-correlated cortical networks arise from spontaneous neuronal dynamics at slow timescales

“…The anti-correlated networks reported here may be extended to a behavioral context when considering the distinct exploratory modes of the rodent, which shift between feedforward sensation and top-down control configurations on a timescale of seconds. These configurations correspond with active sensing and anticipatory behavioral states 15 , 16 and are layer-specific 45 : early activation of deep layers correlates with anticipatory behavior, whereas early activation of superficial layers correlates with active sensing 17 . The rodent’s ability to switch between these behavioral modes is critical since each mode involves the mutually exclusive use of subcortical brain structures and peripheral resources.…”

Transition between functional regimes in an integrate-and-fire network model of the thalamus

“…In contrast, in the awake state TC neurons are known to vary their activity according to inputs coming from the associated receptor layers, and to affect in turn the activity of the associated primary sensory cortex. For instance, TC neurons belonging to the lateral geniculate nucleus (LGN) and the ventral posterior nucleus (VPN) are modulated by the retina [14] and by the tactile afferents [15], respectively, and modulate in turn the activity of primary visual and somatosensory cortical areas [4,16,17]. TC neurons are also key components of the above-mentioned gating role of the thalamus, contributing to the selection of salient information during selective attention [10].…”