(dis)organizational principles for neuronal responses in the whisker system

Rodents use their whiskers to perform demanding sensory discrimination tasks. Identifying an object's position or texture requires the system to encode temporal patterns of whisker motion fluctuations with high precision. Accordingly, neurons in the somatosensory thalamus and cortex are not just sensitive to spatial stimulus structure -e.g., motion of particular whiskers or in particular directions-, but also have clear feature selectivity (receptive fields) in the temporal domain. Here I will describe recent work in search of the principles governing this feature selectivity.

Different neurons in the barrel cortex participate heterogeneously in a given sensory task -e.g., texture discrimination. The highly variable representation across single neurons coexists with a robust code for texture at the level of small populations. The robustness of the population signal is explained by synergistic interactions between neurons carrying stronger and weaker signals; the variability across single neurons can be partly understood in terms of neurons within a given processing stage having highly diverse temporal feature selectivity. This diversity appears uncoordinated with any aspect of whisker somatotopy. As a consequence, a wide range of response properties can be sampled within a small region of barrel cortex.

Diverse temporal feature selectivity is also found in the VPM nucleus, the main thalamic relay to cortex: different VPM neurons respond to distinct stimulus features. The existence of rich, diverse population codes at both thalamic and cortical stages raises the question of how information is successfully transmitted under conditions where the heterogeneity of thalamic neurons manifests itself - i.e., where thalamic responses are not overwhelmingly synchronous. I will present ongoing work suggesting the feasibility of a mode of communication where partially synchronous thalamic activity could suffice to influence cortical neurons. Specifically, in slice experiments we have found that thalamocortical synapses have strikingly heterogeneous short-term plasticity during ongoing stimulation: each synapse responds most strongly to particular stimulation intervals, giving rise to a rich "synaptic population code" for dynamic stimuli.