Contextual modulation of behavioral choice

Abstract

We review the influence of context on behavioral choice. Context can refer to external (environmental) factors such as the season or presence of predators and it can also refer to the internal or behavioral state of an animal. Usually, animals make decisions in the midst of other ongoing behaviors. We discuss recent findings on the impact of both types of contexts, focusing on how context gets encoded at the intersection between the sensory and motor systems, emphasizing the role of neuromodulators. We also review recent technological advances that have made feasible the exploration of neural correlates of decision making in freely moving, behaving animals.

Figure 1. Summary of contextual modulation of behavioral choice

Stimuli are processed by the nervous system in a manner that elicits a behavioral response. External (left column) and internal (right column) contexts can have a significant impact on the choice of behavior. Context can be encoded through functional circuitry or through the modulation of specific neuromodulators (represented here by color; see key). Context can affect (1) the encoding or decoding of stimuli (represented here by arrows extending to the “sensory” compartment); (2) the activity of the motor system (represented here by arrows extending to the “motor” compartment); or (3) have a more systemic affect on the nervous system (represented here by arrows extending to the “nervous system” compartment). Numbers next to contexts indicate reference number. For example, when leeches are engaged in feeding (an internal context) [ref 44], serotonin (represented by red arrow) presynaptically inhibits connections between sensory cells (represented by arrow extending to the “sensory” compartment) and interneurons that mediate other behaviors, leading to a noticeable modulation of behavioral choice.

Figure 2. Behavioral state influences processing of sensory information

(a) Feeding in the medicinal leech decreases the excitatory post-synaptic potential (EPSP) amplitude of a local bend interneuron (cell 212) elicited by spikes in a pressure sensitive mechanosensory cell (P cell). Cell 212 is involved in the production of a local bending behavior in the leech. The inset shows three overlaid traces from cell 212 illustrating the responses to P cell stimulation in pre-feeding, feeding, and post-feeding time periods (scale bars = 20 mV and 100 ms). Modified from [44••]. (b) Average power spectrum of local field potential (LFP) response in mouse primary visual cortex to drifting, oriented bars while the head fixed mouse was stationary (red trace) or running on a floating track ball (blue trace). The amplitudes of the signals at different frequencies change significantly when the animal was moving. Reprinted with permission from [59•]. (c) Membrane voltage, measured with patch clamp, of one motion sensitive VS (vertical-system) interneuron in Drosophila before (red), during (blue), and after (black) flight. The synaptic inputs onto VS interneurons increased during flight. Directions (L– left; R – right; D – down; DL – down left; DR – down right; U – up; UL – up left; UR – up right) refer to motion of drifting grating visual stimulus. Reprinted with permission from [50••]. (d) Two-photon calcium imaging of a single motion sensitive HS (horizontal-system) interneuron in Drosophila during walking (red trace) or at rest (blue trace). The visual responses of the HS cell increased dramatically in response to gratings drifting in the cell’s preferred direction (PD), but not in the null direction (ND). Reprinted with permission from [51].