Sensation, movement and learning in the absence of barrel cortex

Abstract

For many of our senses, the role of the cerebral cortex in detecting stimuli is controversial. Here we examine the effects of both acute and chronic inactivation of the primary somatosensory cortex in mice trained to move their large facial whiskers to detect an object by touch and respond with a lever to obtain a water reward. Using transgenic mice, we expressed inhibitory opsins in excitatory cortical neurons. Transient optogenetic inactivation of the primary somatosensory cortex, as well as permanent lesions, initially produced both movement and sensory deficits that impaired detection behaviour, demonstrating the link between sensory and motor systems during active sensing. Unexpectedly, lesioned mice had recovered full behavioural capabilities by the subsequent session. This rapid recovery was experience-dependent, and early re-exposure to the task after lesioning facilitated recovery. Furthermore, ablation of the primary somatosensory cortex before learning did not affect task acquisition. This combined optogenetic and lesion approach suggests that manipulations of the sensory cortex may be only temporarily disruptive to other brain structures that are themselves capable of coordinating multiple, arbitrary movements with sensation. Thus, the somatosensory cortex may be dispensable for active detection of objects in the environment.

The influence of visual cortex on perception is modulated by behavioural state

“…When the task is easy to solve then alternative pathways and downstream networks are likely already optimally engaged, and cortical stimulation represents a distractor. Our results parallel recent findings from lesion and silencing experiments 26 showing that learned tasks are no longer cortically dependent and additionally suggest that cortical resources are dynamically allocated depending on task difficulty and performance. Our findings differ from a recent study 64 which found that photostimulation at just two cell locations could recruit an associated ensemble which then always positively biased stimulus perception.…”

“…Moreover, since the local and downstream network activity resulting from the manipulation have typically not been recorded, mechanistically linking the manipulation and behaviour via circuit dynamics has previously not been possible. Another complication is that silencing [19][20][21] and lesion [22][23][24][25] experiments have in some cases produced contradictory findings about the requirement for cortical activity in perception and behaviour 26,27 . The modulation of cortical responses by behavioural state [28][29][30][31] , task outcome 32 and task demands 33,34 have been well reported.…”

Effects of arousal and movement on secondary somatosensory and visual thalamus

“…To test this, we expressed halorhodopsin in all excitatory cortical neurons by crossing Emx1-Cre mice with a Cre-condition halorhodopsin responder line. We recently demonstrated that this technique could block 95-100% of action potentials throughout all cortical layers of awake behaving mice (Hong et al 2018). We recorded from POm cells and, for comparison, VPM cells while silencing S1 or M1 with an amber laser.…”

Absence epilepsy might build its own nest

“…A recent study by Hong et al . (), which showed that even in the complete absence of barrel cortex mice are capable of performing whisker‐related tasks, provides a cautionary note. In light of this, it is possible that the methods used by Studer et al .…”

“…Despite the altered microstructure and evoked potential kinetics, no difference between GAERS and non-epileptic Wistar rats in a texture discrimination test was detectable, and therefore the authors suggest that the sensory circuits of the somatosensory cortex are still able to process whisker-related information. A recent study by Hong et al (2018), which showed that even in the complete absence of barrel cortex mice are capable of performing whisker-related tasks, provides a cautionary note. In light of this, it is possible that the methods used by Studer et al (2019) might underestimate the functional impairment of somatosensory cortex, given that other brain regions are able to compensate for the missing or non-functional somatosensory cortex.…”