Behaviour-dependent recruitment of long-range projection neurons in somatosensory cortex

Abstract

In the mammalian neocortex, segregated processing streams are thought to be important for forming sensory representations of the environment, but how local information in primary sensory cortex is transmitted to other distant cortical areas during behaviour is unclear. Here we show task-dependent activation of distinct, largely non-overlapping long-range projection neurons in the whisker region of primary somatosensory cortex (S1) in awake, behaving mice. Using two-photon calcium imaging, we monitored neuronal activity in anatomically identified S1 neurons projecting to secondary somatosensory (S2) or primary motor (M1) cortex in mice using their whiskers to perform a texture-discrimination task or a task that required them to detect the presence of an object at a certain location. Whisking-related cells were found among S2-projecting (S2P) but not M1-projecting (M1P) neurons. A higher fraction of S2P than M1P neurons showed touch-related responses during texture discrimination, whereas a higher fraction of M1P than S2P neurons showed touch-related responses during the detection task. In both tasks, S2P and M1P neurons could discriminate similarly between trials producing different behavioural decisions. However, in trials producing the same decision, S2P neurons performed better at discriminating texture, whereas M1P neurons were better at discriminating location. Sensory stimulus features alone were not sufficient to elicit these differences, suggesting that selective transmission of S1 information to S2 and M1 is driven by behaviour.

Pathway-specific reorganization of projection neurons in somatosensory cortex during learning

“…6a-c). Among these neurons, we also observed a small number of neurons whose activity correlated to whisking amplitude during active whisking 8,22 (data not shown), but classified these neurons as being non-touch for the purposes of this study.…”

“…'Misses' on go trials were not rewarded. In our previous study 8 , 'false alarms' on no-go trials were punished with an air puff against the whisker pad and a time out period. Here, only a time out period was used to avoid contaminating neuronal activity by air puff-driven whisker deflections, allowing us to compare texture-touch activity between correct rejection and false alarm trials.…”

“…Previous studies have demonstrated that these two subpopulations differ functionally in their intrinsic excitability and in their responses to whisker stimulation during both anesthetized and awake conditions 9,10 . In trained mice performing whiskerbased discrimination tasks, we found that S2P and M1P neurons functionally differ in a task-dependent manner: S2P neurons were prominently recruited and more relevant during texture discrimination, whereas M1P neurons showed increased responsiveness and discriminative power during object localization 8 . Thus, S1 is capable of conveying different streams of information to M1 and S2 during task performance.…”

“…Such information processed in S1 is transferred to other brain areas through excitatory long-range projection neurons. In layer 2/3 (L2/3) of S1, cortico-cortical neurons predominate 6 with M1-projecting (M1P) and S2-projecting (S2P) neurons representing two large, non-overlapping subpopulations [7][8][9][10] . Previous studies have demonstrated that these two subpopulations differ functionally in their intrinsic excitability and in their responses to whisker stimulation during both anesthetized and awake conditions 9,10 .…”

Cortical fosGFP Expression Reveals Broad Receptive Field Excitatory Neurons Targeted by POm

“…Recently, axonal projection targets have been used to differentiate between layer 2/3 barrel cortex pyramidal neurons in behaving mice (Chen et al, 2013;Yamashita et al, 2013). Here we used fosGFP as a marker for layer 2/3 pyramidal neurons, which appear to project with similar likelihood to M1, S2, and contralateral S1 ( Figure S4).…”