Abstract
Goal-directed behavior involves distributed neuronal circuits in the mammalian brain, including diverse regions of neocortex. However, the cellular basis of long-range cortico-cortical signaling during goal-directed behavior is poorly understood. Here, we recorded membrane potential of excitatory layer 2/3 pyramidal neurons in primary somatosensory barrel cortex (S1) projecting to either primary motor cortex (M1) or secondary somatosensory cortex (S2) during a whisker detection task, in which thirsty mice learn to lick for water reward in response to a whisker deflection. Whisker stimulation in 'Good performer' mice, but not 'Naive' mice, evoked long-lasting biphasic depolarization correlated with task performance in S2-projecting (S2-p) neurons, but not M1-projecting (M1-p) neurons. Furthermore, S2-p neurons, but not M1-p neurons, became excited during spontaneous unrewarded licking in 'Good performer' mice, but not in 'Naive' mice. Thus, a learning-induced, projection-specific signal from S1 to S2 may contribute to goal-directed sensorimotor transformation of whisker sensation into licking motor output.
Highlights
Primary sensory cortex processes incoming sensory information flexibly in an experience, context and task-dependent manner (Gilbert and Li, 2013; Harris and Mrsic-Flogel, 2013)
Thirsty mice were trained to lick for water reward in response to a 1 ms deflection of the right C2 whisker (Sachidhanandam et al, 2013; Sippy et al, 2015), and whole-cell Vm recordings were targeted through two-photon microscopy to fluorescently-labelled M1-p and S2-p neurons in layer 2/3 of the C2 barrel column in S1 of the left hemisphere (Yamashita et al, 2013) (Figure 1A,B)
Box plots for postsynaptic potential (PSP) amplitude, secondary late Vm depolarization quantified at 0.05–0.25 s, Vm depolarization during the lick period, and evoked action potential (AP) rates at early (0–0.05 s), late (0.05–0.25 s) and lick (0.25–1.0 s) periods
Summary
Primary sensory cortex processes incoming sensory information flexibly in an experience, context and task-dependent manner (Gilbert and Li, 2013; Harris and Mrsic-Flogel, 2013). Functionallytuned sensory information is signaled from primary sensory cortex to distinct cortical areas (Movshon and Newsome, 1996; Sato and Svoboda, 2000; Chen et al, 2013; Glickfeld et al, 2013; Yamashita et al, 2013), but the cellular mechanisms underlying specific cortico-cortical signals during goal-directed behavior are poorly understood. Neuronal activity in primary somatosensory barrel cortex (S1) is known to participate in the execution of a simple whisker-dependent detection task, in which thirsty mice learn to lick a spout in order to obtain a water reward (Sachidhanandam et al, 2013). Retrograde labeling suggests that M1-p and S2-p neurons in S1 are largely non-overlapping types of excitatory
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