Synaptic Mechanisms Underlying Sparse Coding of Active Touch

Abstract

Sensory information is actively gathered by animals, but the synaptic mechanisms driving neuronal circuit function during active sensory processing are poorly understood. Here, we investigated the synaptically driven membrane potential dynamics during active whisker sensation using whole-cell recordings from layer 2/3 pyramidal neurons in the primary somatosensory barrel cortex of behaving mice. Although whisker contact with an object evoked rapid depolarization in all neurons, these touch responses only drove action potentials in ∼10% of the cells. Such sparse coding was ensured by cell-specific reversal potentials of the touch-evoked response that were hyperpolarized relative to action potential threshold for most neurons. Intercontact interval profoundly influenced touch-evoked postsynaptic potentials, interestingly without affecting the peak membrane potential of the touch response. Dual whole-cell recordings indicated highly correlated membrane potential dynamics during active touch. Sparse action potential firing within synchronized cortical layer 2/3 microcircuits therefore appears to robustly signal each active touch response.

Inhibitory Plasticity Balances Excitation and Inhibition in Sensory Pathways and Memory Networks

“…2 D, E.) In the detailed balanced state (established by inhibitory plasticity), the response of the cell is sparse (Fig. 2 B, lower panels) and reminiscent of experimental observations (20,(27)(28)(29)(30)) across many sensory systems. Action potentials are caused primarily by transients in the input signals, during which the faster dynamics of the excitatory synapses momentarily overcome inhibition.…”

Time in Cortical Circuits

“…We noted above that the synaptic latency changes little during short-term synaptic plasticity (Barnes et al, 2015). Furthermore, synaptic latency is preserved during experience-dependent plasticity, when changes in synaptic strength are accompanied by structural changes at synapses (Cheetham et al, 2008;Cheetham et al, 2014;Barnes et al, 2015).…”

“…The questions focus on the temporal properties of signaling between cortical neurons, how that signaling can be modified, and what the signaling may contribute to time-dependent cognition. Building from the top down, we consider cognitive processes that involve time as we perceive it (Fraisse, 1964(Fraisse, , 1984Allman et al, 2014). We focus on cognitive processes that operate in the present or anticipate events or stimuli in the near future.…”

“…There are excellent reviews on the role of internal clocks in time perception (Allman et al, 2014). Similarly, numerous insightful reviews discuss the past and memory (Martin et al, 2000;Frankland and Bontempi, 2005;Silva et al, 2009).…”

“…The time taken for the entire series of events is referred to as the synaptic latency. Despite the multiplicity of processes, the synaptic latency usually remains relatively constant for any given connection in mature cortex, even when the connection is activated repeatedly (Ͻ40 Hz) (Barnes et al, 2015). The time course of the excitatory postsynaptic response is modified by factors intrinsic to the postsynaptic neuron (e.g., passive membrane properties, ion channel distribution) and by inhibition.…”