Whisking-Related Changes in Neuronal Firing and Membrane Potential Dynamics in the Somatosensory Thalamus of Awake Mice

Abstract

The thalamus transmits sensory information to the neocortex and receives neocortical, subcortical, and neuromodulatory inputs. Despite its obvious importance, surprisingly little is known about thalamic function in awake animals. Here, using intracellular and extracellular recordings in awake head-restrained mice, we investigate membrane potential dynamics and action potential firing in the two major thalamic nuclei related to whisker sensation, the ventral posterior medial nucleus (VPM) and the posterior medial group (Pom), which receive distinct inputs from brainstem and neocortex. We find heterogeneous state-dependent dynamics in both nuclei, with an overall increase in action potential firing during active states. Whisking increased putative lemniscal and corticothalamic excitatory inputs onto VPM and Pom neurons, respectively. A subpopulation of VPM cells fired spikes phase-locked to the whisking cycle during free whisking, and these cells may therefore signal whisker position. Our results suggest differential processing of whisking comparing thalamic nuclei at both sub- and supra-threshold levels.

Mechanisms underlying a thalamocortical transformation during active tactile sensation

“…VPM neurons were also highly sensitive to whisking (Fig 2b and 2c) [17, 18, 21]. Spike rates increased after whisking onset (average, 3-fold; Fig 1c and 1d).…”

“…During active sensation, movement of the sensors produces ‘reafferent’ signals, whereas interactions with the world generate ‘exafferent’ signals. During haptic exploration, movement activates peripheral sensors to produce reafference and touch generates exafference [15–21]. The brain needs to parse these different signals for perception [13].…”

“…Neurons in VPM respond to touch, but they also increase their activity during whisker movement (‘whisking’) [17–21]. L4 FS neurons have nearly identical dynamics as VPM neurons.…”

Movement Initiation Signals in Mouse Whisker Motor Cortex

“…AP firing (Curtis and Kleinfeld, 2009) and V m fluctuations in wS1 (Crochet and Petersen, 2006) correlate with rhythmic whisker movements. In wS1, these phase-locked oscillations are abolished upon transecting the infraorbital nerve, indicating that the source of these fluctuations might be re-afferent signals from the periphery (Poulet and Petersen, 2008), presumably relayed via the primary somatosensory ventral posterior medial (VPM) thalamic nucleus (Moore et al., 2015, Urbain et al., 2015). Interestingly, phase-locked fluctuations in wM1-projecting neurons of wS1 are significantly larger than those in wS2-projecting neurons of wS1 (Yamashita et al., 2013).…”

T-type calcium channels in synaptic plasticity

“…However, it is now clear that in some brain areas, the density of T-type channels expressed in neurons is high enough to allow a significant number of deinactivated T-type channels at the membrane potentials reported in awake animals. 88 For example, in the thalamus, the fraction of T-type channels that is available at depolarized potential participates to EPSP amplification and has a drastic effect on spike probability during wake states. 89 Second, the lack of suitable T-type channel antagonists has hampered for many years the discovery of subtle functions for neuronal T-type currents and made impossible to definitely prove their implication in synaptic plasticity.…”