The neural substrates of deliberative decision making: contrasting effects of hippocampus lesions on performance and vicarious trial-and-error behavior in a spatial memory task and a visual discrimination task

Abstract

Vicarious trial-and-errors (VTEs) are back-and-forth movements of the head exhibited by rodents and other animals when faced with a decision. These behaviors have recently been associated with prospective sweeps of hippocampal place cell firing, and thus may reflect a rodent model of deliberative decision-making. The aim of the current study was to test whether the hippocampus is essential for VTEs in a spatial memory task and in a simple visual discrimination (VD) task. We found that lesions of the hippocampus with ibotenic acid produced a significant impairment in the accuracy of choices in a serial spatial reversal (SR) task. In terms of VTEs, whereas sham-lesioned animals engaged in more VTE behavior prior to identifying the location of the reward as opposed to repeated trials after it had been located, the lesioned animals failed to show this difference. In contrast, damage to the hippocampus had no effect on acquisition of a VD or on the VTEs seen in this task. For both lesion and sham-lesion animals, adding an additional choice to the VD increased the number of VTEs and decreased the accuracy of choices. Together, these results suggest that the hippocampus may be specifically involved in VTE behavior during spatial decision making.

Vicarious trial and error

“…Although it is true that rats have a very wide field of view, VTE has been observed in walled-maze tasks in which the animal cannot see the goal 56,87 , so any sensory-information-gathering theory would have to depend on only the first part of a journey. Moreover, VTE-like reorientations observed in sensory-information-gathering situations do not depend on hippocampal integrity, unlike VTE-like reorientations in goal-directed behaviours 86 . VTE is more likely to be a reflection of an internal process 50,58 , perhaps as the halted initiation of an action.…”

Conflict between place and response navigation strategies: Effects on vicarious trial and error (VTE) behaviors

“…In contrast, once the food reward was found, the animals showed less VTE on successive trials. This was not the case for hippocampal-lesioned rats, which showed lower levels of VTE before finding the reward, but, unlike controls, did not show a decrease in VTE behavior on subsequent trials (Bett et al 2012). Bett et al's results complement our study by suggesting that while VTE is greater when rats are engaged in strategies that are hippocampal-dependent, this does not necessitate that VTE is strictly a hippocampal process.…”

“…First of all, hippocampal tasks such as place navigation also involve other structures (Whishaw et al 1987;Packard et al 1994;Devan and White 1999;Voss et al 2011;Gruber and McDonald 2012). Although some studies have shown impairments in VTE and performance with hippocampal lesions (Hu and Amsel 1995), VTE has also been seen on hippocampusindependent tasks (Bett et al 2012). The study by Bett and colleagues showed a more subtle relationship between the hippocampus and VTE behavior.…”

Covert rapid action-memory simulation (CRAMS): A hypothesis of hippocampal–prefrontal interactions for adaptive behavior

“…VTE is high early in learning and when the choice is most uncertain, reflecting difficulty at arriving at a conclusion based on simulation, and becomes less frequent with learning and increased certainty (Tolman, 1932, 1938, 1939). Furthermore, several experiments have shown that VTE is reduced with lesions of the hippocampus (Hu and Amsel, 1995), especially when VTE is generated in tasks requiring the use of memory of previous episodes to select between the two behavioral choices, such as in two-arm maze tasks as opposed to two-choice perceptual discrimination tasks (Bett et al, 2012). Johnson and Redish (2007) found that hippocampal CA1 neurons generate non-local firing patterns at the choice point in a T-maze, where VTE is generated.…”