Global Representations of Goal-Directed Behavior in Distinct Cell Types of Mouse Neocortex

Abstract

SUMMARYThe successful planning and execution of adaptive behaviors in mammals may require long-range coordination of neural networks throughout cerebral cortex. The neuronal implementation of signals that could orchestrate cortex-wide activity remains unclear. Here, we develop and apply methods for cortex-wide Ca2+ imaging in mice performing decision-making behavior and identify a global cortical representation of task engagement encoded in the activity dynamics of both single cells and superficial neuropil distributed across the majority of dorsal cortex. The activity of multiple molecularly defined cell types was found to reflect this representation with type-specific dynamics. Focal optogenetic inhibition tiled across cortex revealed a crucial role for frontal cortex in triggering this cortex-wide phenomenon; local inhibition of this region blocked both the cortex-wide response to task-initiating cues and the voluntary behavior. These findings reveal cell-type-specific processes in cortex for globally representing goal-directed behavior and identify a major cortical node that gates the global broadcast of task-related information.

Three brain states in the hippocampus and cortex

“…Research in sensory cortex has traditionally eliminated or isolated self‐generated movement. Other work has addressed the direct contribution of internally routed motor signals (Allen et al, ; Busse et al, ; Eliades & Wang, ; Fanselow & Nicolelis, ; Fee, Mitra, & Kleinfeld, ; Lee, Hoy, et al, ; Lee, Kruglikov, Huang, Fishell, & Rudy, ; Nelson et al, ; Petreanu et al, ; Schneider et al, ), particularly with respect to perceptual stability (Hall & Colby, ; Kleinfeld, Ahissar, & Diamond, ; Kleinfeld, Berg, & O'Connor, ; Sommer & Wurtz, ; Wurtz, Joiner, & Berman, ). This focus has led to valuable insights but may also be limited in the premise that, during movement, cortex functions to construct a single factual representation.…”

Top‐down and bottom‐up control of stress‐coping

“…To translate these specific types of behaviour into neural mechanisms, it is important to better understand the underlying circuitry responsible for proper execution of behavioural output, especially as different types of behaviour often correspond to distinct functional groups of neurones. 206 Previous work indicates that both the prelimbic and infralimbic cortex are important for anticipatory behaviour. 204 The mPFC can be organised into increasingly narrow functional units, based on their location, cell type or projection target.…”

Embedded ensemble encoding hypothesis: The role of the “Prepared” cell

“…Experimental measurements show that the distribution of neurons involved in one functional neural ensemble is not restricted to the cerebral cortex, but it is likely to include subcortical gray matter (Figure c, amygdala and hippocampus) (Brecht, Singer, & Engel, ; Ziaei, Peira, & Persson, ). Cortex‐wide Ca 2+ imaging in mice performing decision‐making behavior revealed robust activation of neurons distributed across the majority of dorsal cortex (Allen et al, ). In summary, these activated groups of cells are widely distributed across different areas of the brain, each specialized in signaling a different attribute of the object or different element within the scene (Mountcastle, ; Perrett, Rolls, & Caan, ; Singer, ; Yu & Ferster, ).…”

“…The ensemble made of neurons in Active state (E_Act, red) is just a subset of the ensemble of neurons in Prepared state (E_Pr, yellow), which itself is a subset of neurons in the OFF state (E_off, gray) neurons involved in one functional neural ensemble is not restricted to the cerebral cortex, but it is likely to include subcortical gray matter ( Figure 3c, amygdala and hippocampus) (Brecht, Singer, & Engel, 1998;Ziaei, Peira, & Persson, 2013). Cortex-wide Ca 21 imaging in mice performing decision-making behavior revealed robust activation of neurons distributed across the majority of dorsal cortex (Allen et al, 2017).…”