Transformation of primary sensory cortical representations from layer 4 to layer 2

Abstract

Sensory input arrives from thalamus in cortical layer (L) 4, which outputs predominantly to superficial layers. L4 to L2 thus constitutes one of the earliest cortical feedforward networks. Despite extensive study, the transformation performed by this network remains poorly understood. We use two-photon calcium imaging to record neural activity in L2-4 of primary vibrissal somatosensory cortex (vS1) as mice perform an object localization task with two whiskers. Touch responses sparsen and become more reliable from L4 to L2, with nearly half of the superficial touch response confined to ~1 % of excitatory neurons. These highly responsive neurons have broad receptive fields and can more accurately decode stimulus features. They participate disproportionately in ensembles, small subnetworks with elevated pairwise correlations. Thus, from L4 to L2, cortex transitions from distributed probabilistic coding to sparse and robust ensemble-based coding, resulting in more efficient and accurate representations.

Representational drift in barrel cortex is receptive field dependent

“…We find that broadly tuned neurons -bidirectional single whisker and especially multiwhisker neurons -are more stable than narrowly tuned single whisker neurons. From L4 to L2, representations of whisker touch transition from narrow to broad tuning and from distributed to ensemble based coding 20 . This cross-laminar receptive field broadening is found in many sensory cortices [17][18][19]41 .…”

“…Following segmentation, neuropil subtraction and ΔF/F computation were performed. For layer assignment, each neuron was first assigned a depth in reference to a single reference plane taken at the top of the dura 20 . The L1-L2 border was defined at the depth of the most superficially imaged excitatory neuron and the L3-L4 border was found by manually locating a noticeable shift in neuron morphology in conjunction with the emergence of clearly visible septa.…”

“…Cortical columns 15 transform sensory input arriving from the thalamus via a feedforward network from L4 to L2 16 , most prominently resulting in receptive field broadening [17][18][19] . In primary vibrissal somatosensory cortex (vS1), representation of whisker touch transitions from a distributed population of narrowly tuned neurons in layer (L) 4 to a sparser ensemble-based representation consisting of correlated neurons with broader tuning in L2 20 . A key function of early sensory cortical processing may therefore be to transition from a more unstable population of narrowly tuned neurons in L4 to a more stable population of broadly tuned neurons in L2, providing a more reliable code for downstream readout 13 .…”

“…We ask whether the transition to broader tuning and greater pairwise correlations from L4 to L2 is accompanied by greater long-term stability among touch neurons. We re-analyze volumetric two-photon calcium imaging 21 data from published experiments 20 in which we monitored touch neurons longitudinally in well-trained mice stably performing an object localization task with two whiskers. We find that neurons with narrower tuning, as well as neurons in L4, show lower levels of stability than more broadly tuned superficial neurons.…”

Input-specific synaptic depression shapes temporal integration in mouse visual cortex

“…Our findings provide long sought-after evidence for a synaptic depression mechanism at intracortical synapses that generates sensory adaptation and sparsens representations. Given the similarity of cortical structure and observed features of rapid adaptation across sensory areas, this mechanism could be applicable across many stimulus modalities 9,[72][73][74] . Release probability is an inherent property at chemical synapses in the brain 11 ; thus, molecular machinery and neuromodulators that affect Pr can regulate synaptic transmission at a given set of synapses over time (as we've studied here), but could also specialize the dynamics of responses across different brain areas, or even different species.…”