Contextual behavior and neural circuits

Abstract

Animals including humans engage in goal-directed behavior flexibly in response to items and their background, which is called contextual behavior in this review. Although the concept of context has long been studied, there are differences among researchers in defining and experimenting with the concept. The current review aims to provide a categorical framework within which not only the neural mechanisms of contextual information processing but also the contextual behavior can be studied in more concrete ways. For this purpose, we categorize contextual behavior into three subcategories as follows by considering the types of interactions among context, item, and response: contextual response selection, contextual item selection, and contextual item-response selection. Contextual response selection refers to the animal emitting different types of responses to the same item depending on the context in the background. Contextual item selection occurs when there are multiple items that need to be chosen in a contextual manner. Finally, when multiple items and multiple contexts are involved, contextual item-response selection takes place whereby the animal either chooses an item or inhibits such a response depending on item-context paired association. The literature suggests that the rhinal cortical regions and the hippocampal formation play key roles in mnemonically categorizing and recognizing contextual representations and the associated items. In addition, it appears that the fronto-striatal cortical loops in connection with the contextual information-processing areas critically control the flexible deployment of adaptive action sets and motor responses for maximizing goals. We suggest that contextual information processing should be investigated in experimental settings where contextual stimuli and resulting behaviors are clearly defined and measurable, considering the dynamic top-down and bottom-up interactions among the neural systems for contextual behavior.

Keywords: choice behavior; context; decision making; entorhinal cortex; hippocampus; perirhinal cortex; post-rhinal cortex; response selection.

Figure 1

A cartoon for illustrating the importance of contextual interpretation of items for choice behavior. Rodents usually avoid novel objects (cheese over the trap in this example) paired with a surrounding context to stay away from danger.

Figure 2

Categorization of contextual behavior. Contextual behaviors are grouped into three categories in this review depending on the relationships among context, item, and the animal's response pattern to the combination of the two. A surrounding context is symbolized as the color-gradient background here. Contextual response selection: an animal produces different types of responses (e.g., pushing vs. digging) to the same item depending on which context is associated with the item. Contextual item selection: an animal gives out the same type of responses to different items depending on the contextual information. Contextual item–response selection: an animal responds to an item (e.g., black item) when it is identified in one context (e.g., orange context), but not when it is encountered in another context (e.g., blue context), and vice versa for the other item (e.g., white item).

Figure 3

A contextual response-selection task. Visual context is defined by the configuration (parameterized by the angular distance) of the two curtains (each with a distinct set of visual cues as shown in the pictures). For example, context A is defined by the two cue-curtains aligned at the center (thick arc lines) and context B is when the two cue-curtains set apart by a larger degree (dotted arc lines).

Figure 4

A touchscreen-based contextual response-selection task. A side view of the LCD-touchscreen apparatus in which two peripheral LCD screens (only one visible from this particular angle) and the center touchscreen (showing two adjacent response target rectangles) were installed to make the rat to choose a particular response using the surrounding visual context (zebra pattern in this example). The LEDs and tether attached to the rat are for electrophysiological recording.

Figure 5

A contextual response-selection task. The rat is required to either dig the sand in the sand-filled jar or push the jar to obtain a piece of cereal. The behavior selection is associated with the visual context presented in the background using an array of three LCD monitors (partially shown here).

Figure 6

An illustration of regions of interest in human VR contextual response-selection task. Human brain regions (color-coded) that are consistently activated in contextual response-selection studies. (A) A posterior view of the brain. Regions of interest (left hemisphere only) were overlaid with the translucent whole brain. (B) A medial view of the same areas shown in (A). The regions associated with the colors closer to violet are sensory and associational cortex (lateral occipital complex, lingual and fusiform gyri). The regions in green spectrum (inferior/superior parietal lobules, precuneus, retrosplenial cortex, and caudate) are the areas that are also frequently activated in a VR navigation task.

Figure 7

A contextual item-selection task. The task requires the rat to choose one of the objects (inset: toy figures) depending on where in the maze the two objects appear. The surrounding visual cues on the curtains serve as a visual context.

Figure 8

An object-cued response selection task. The rat exits the start box and runs along the linear track and encounters an object cue (orange toy figure in this example). The object signals which disc on its left or right side should be displaced for successful retrieval of food. Rats are impaired in this task when the distal visual cues in the background are removed (by darkening the room).

Figure 9

A schematic illustration of the information flow and interactions among the brain regions (selectively chosen) involved in contextual behavior (connections are simplified for illustrative purposes). Via primary and higher-order sensory cortices (SCx), multimodal perceptual information from the environment enters the rhinal cortical regions (RhCx) that include the post-rhinal cortex (POR), perirhinal cortex (PER), medial entorhinal cortex (MEC), and lateral entorhinal cortex (LEC). The areas in the RhCx may interact with each other to varying degrees as indicated by arrows. It is hypothesized that qualitatively different information-processing streams exist in the RhCx, denoted by red arrows (contextual information) and blue arrows (item information) here. The qualitatively different information streams continue as the information enters the hippocampal formation (HPF) in which associative processes occur between these two streams (presumably in order to form an event representation). The hippocampal subfields (DG, CA3, CA1) and subiculum (SUB) all receive contextual-noncontextual information in parallel. Serial information processing across the hippocampal subfields to SUB also occurs at the same time. The DG-CA3 network (circular arrow indicating the recurrent network in CA3) is particularly important for recognizing ambiguous/modified contexts in comparison to memory representations (e.g., rat discriminating different visual contexts modified from the original ones). The information regarding the contextual interpretation of the environment and its associated items then interacts with the fronto-striatal networks (FSL) including the prefrontal cortex (PFC) and striatum (STR) in a goal-directed manner before final response behavior is determined (e.g., digging in pebble context here). The four regions (SCx, RhCx, HPF, and FSL) interact with each other via various feedforward and feedback connections to realize coherent, inter-regional bottom-up and top-down communications toward goal-directed behavior.