Sensorimotor processing in the rodent barrel cortex

Abstract

Tactile sensory information from facial whiskers provides nocturnal tunnel-dwelling rodents, including mice and rats, with important spatial and textural information about their immediate surroundings. Whiskers are moved back and forth to scan the environment (whisking), and touch signals from each whisker evoke sparse patterns of neuronal activity in whisker-related primary somatosensory cortex (wS1; barrel cortex). Whisking is accompanied by desynchronized brain states and cell-type-specific changes in spontaneous and evoked neuronal activity. Tactile information, including object texture and location, appears to be computed in wS1 through integration of motor and sensory signals. wS1 also directly controls whisker movements and contributes to learned, whisker-dependent, goal-directed behaviours. The cell-type-specific neuronal circuitry in wS1 that contributes to whisker sensory perception is beginning to be defined.

Part a is adapted from Matyas et al., 2010 (Ref #109).

Fig. 1. Long-range connectivity of wS1 barrel cortex.

a | The primary somatosensory cortex of rats and mice contains obvious anatomical units called ‘barrels’ in layer 4 of wS1, which represent individual whiskers on the snout and are somatotopically organized. b | Deflection of a mystacial whisker evokes sequential activity in: trigeminal ganglion primary sensory neurons (1); brainstem neurons (2); and thalamic neurons (3), before reaching wS1. c | A schematic representation of the long-range connectome of wS1^–. Red font highlights strongly connected brain regions discussed further in this Review. APT, anterior pretectal nucleus; DLS, dorsolateral striatum; DZ, dysgranular zone surrounding wS1; nRT, nucleus reticularis of the thalamus; OFC, orbitofrontal cortex; POm, posterior medial nucleus of the thalamus; PPC, posterior parietal cortex; PRh/TeA, perirhinal cortex or temporal association cortex; SC, superior colliculus; Sp5, spinal trigeminal nuclei; wM1/2, primary/secondary whisker motor cortex; wS1, primary whisker somatosensory barrel cortex; wS2, secondary whisker somatosensory cortex; VPM, ventral posterior medial nucleus of the thalamus; V2 (P, PP), secondary visual area, labelled in previous studies as area P or PP.

Fig. 2. Neural circuits for sparse reliable coding of touch in wS1.

a | Neurons in primary whisker somatosensory thalamus (VPM) signal whisker deflections primarily to L4 barrels (outlined in cyan). VPM axons (blue shading) extend into the L3 regions directly above the L4 barrels. Higher-order thalamic input from POm innervates L1 and L5A. b | Excitatory neuronal microcircuits of wS1 include the ‘canonical’ L4→L2/3→L5 pathway, as well as many other synaptic pathways including L4→L5, L4→L6, L5A→L2, L6→L5A and L5→L6. Extensive horizontal connectivity across barrel columns is prominent in L2/3 and L5/6. c | Fast-spiking inhibitory GABAergic neurons expressing PV are strongly and reciprocally connected to nearby excitatory neurons and also receive thalamic input. PV⁺ neurons provide feedforward, lateral and feedback inhibition. d| Sparse strong excitatory synaptic connectivity combined with strong dense inhibition could drive reliable, sparse activity in specifically wired excitatory neuronal circuits.

Fig. 3. Cell-type-specific modulation in wS1 during active whisking.

Schematic representation of the dynamics of whisker movements and cell-type-specific V_m fluctuations and action potential firing during quiet and whisking periods. During quiet periods, when the whiskers are not moving, slow synchronous V_m fluctuations are found in excitatory (EXC) neurons, PV⁺ neurons and VIP⁺ neurons in L2/3. SST⁺ neurons show smaller V_m fluctuations that are less correlated to their neighbours. During whisking, thalamic action potential firing rates increase and cholinergic inputs (which are labelled in ChAT GCaMP mice) become more active. Slow cortical V_m fluctuations are suppressed during whisking. VIP⁺ neurons depolarize and increase firing rate, whereas SST⁺ neurons hyperpolarize and decrease their action potential rate. b | Schematic synaptic circuitry contributing to state-dependent patterns of L2/3 activity. Cholinergic input might depolarize VIP⁺ neurons, which express nicotinic acetylcholine receptors. VIP⁺ neurons inhibit SST⁺ neurons. Thalamic input (from the VPM or POm) to excitatory neurons and PV⁺ neurons drives depolarized, desynchronized V_m fluctuations, with combined glutamatergic and GABAergic conductances reducing V_m variance in most cell-types.c | A brief whisker deflection evokes an excitatory neuronal response in wS1, which can subsequently propagate to other brain regions such as wM1, as visualized by voltage-sensitive dye (VSD) imaging. Large, spreading sensory responses are evoked during quiet wakefulness, whereas the same whisker deflection evokes a smaller, more localized response if delivered during whisking. d | Single-trial examples of whole-cell V_m recording from a L4 spiny stellate neuron in wS1 showing the sensory response evoked by a whisker deflection during a period of quiet wakefulness and during whisking. Panel c is from Ferezou et al., 2007. Ref #15. Panel d is from Crochet & Petersen, 2006. Ref #12.

Fig. 4. Sensorimotor computations in wS1.

a |Rodents can localize objects with their whiskers, which requires integration of motor and sensory signals. Some neurons in wS1 exhibit rapid V_m fluctuations that are phase-locked to the whisking cycle. In the schematic example, during free whisking, cell 1 is most depolarized when the whisker is in a relatively retracted position, whereas cell 2 is most depolarized at a more protracted whisker position. Whisker–object contact evokes depolarizing sensory postsynaptic potentials (touch PSP). If touch occurs at a retracted phase of whisking, the V_m of cell 1 might cross the threshold required to fire an action potential. By contrast, if touch occurs at a protracted phase, cell 2 might be more likely to fire an action potential. b | Axons from wM1 innervate L1 of wS1. Calcium imaging of the L1 tuft dendrites of L5 pyramidal neurons reveals that active touch evokes signals that are suppressed by inactivation of wM1. The dendrites of different cells respond to different object locations. Panel b is from Xu et al., 2012. Ref #110.

Fig. 5. Neural circuits for goal-directed sensorimotor transformation.

a Some neurons in L2/3 of wS1 project to wS2 (red) and other neurons project to wM1 (blue). Neurons in wS1 projecting to wS2 have a larger depolarizing response to whisker deflection in expert (trained) mice performing a whisker detection task than do naive mice. These neurons also depolarize immediately before ‘false alarm’ licking in expert mice but not naive mice. Neurons in wS1 that project to wS2 might therefore contribute to the transformation of sensory input into the motor command to initiate licking for reward. By contrast, neurons in wS1 that project to wM1 show no such training-dependent differences in false-alarm-related activity.b | Schematic circuit diagram illustrating the hypothesis that reward-based learning of a simple whisker detection task might involve strengthening of reciprocal excitation between wS1 and wS2. How neuronal activity in wS1 and wS2 might ultimately signal to tongue- and jaw-related motor neurons (tjMN) to evoke licking is currently unknown, but presumably involves interactions with many other brain areas. c | Schematic drawing highlighting the potential role of dopamine acting on D1R-expressing direct pathway striatonigral projection neurons (dSPNs) to potentiate glutamatergic input from cortex and/or thalamus through reward-based learning. Enhanced sensory-evoked activity in dSPNs could contribute to evoke licking by disinhibition of brainstem motor nuclei and/or motor thalamus. Panel a is from Yamashita & Petersen, 2016. Ref #137.