Spontaneous revisitation during visual exploration as a link among strategic behavior, learning, and the hippocampus

Abstract

Effective exploratory behaviors involve continuous updating of sensory sampling to optimize the efficacy of information gathering. Despite some work on this issue in animals, little information exists regarding the cognitive or neural mechanisms for this sort of behavioral optimization in humans. Here we examined a visual exploration phenomenon that occurred when human subjects studying an array of objects spontaneously looked "backward" in their scanning paths to view recently seen objects again. This "spontaneous revisitation" of recently viewed objects was associated with enhanced hippocampal activity and superior subsequent memory performance in healthy participants, but occurred only rarely in amnesic patients with severe damage to the hippocampus. These findings demonstrate the necessity of the hippocampus not just in the aspects of long-term memory with which it has been associated previously, but also in the short-term adaptive control of behavior. Functional neuroimaging showed hippocampal engagement occurring in conjunction with frontocerebellar circuits, thereby revealing some of the larger brain circuitry essential for the strategic deployment of information-seeking behaviors that optimize learning.amnesia | prefrontal cortex | vicarious trial-and-error behavior O ne of the hallmarks of higher cognitive functioning is the ability to flexibly tailor behaviors to current situational demands. An example comes from the purposeful way animals explore the environment, effectively sampling the particular information most critical for learning and later memory. A number of investigators have emphasized the critical role in such behaviors of memory systems (1, 2) and strategic/executive control systems (3, 4). Some theorizing about exploratory behaviors has emphasized the potential importance of constant iteration between perception and action (5, 6) or between prediction and verification (7-9). However, little is known, at least in humans, about precisely how processing in neural systems leads to the optimization of exploratory behaviors and how the behaviors, in turn, affect processing in these systems as learning occurs. This is partially because contemporary research often involves exposing individuals to some information and relating brain activity to the ability to later recall or recognize aspects of the original learning event (10). Findings therefore primarily concern processes closely allied with introspective reports rather than the processes by which memory signals are used by the organism in the moment-tomoment guidance of dynamic behavior.Connections between brain activity and ongoing behavior are generally better understood in animals, in which the assaying of active behaviors is a necessity for studying learning and memory.* For the work reported here, one notable example is a phenomenon in rodents described by Muenzinger (13) and Tolman (7-9) that seems to relate memory processing and exploratory behavior. When learning to discriminate between two stimuli based on one item's selective associa...

Unconscious Relational Inference Recruits the Hippocampus

“…Accordingly, only conscious memories are thought to be flexibly integrated and expressed (Reber et al, 1996;Smith and Squire, 2005). However, these classic notions have been questioned by the finding of implicit inference (Greene et al, 2001(Greene et al, , 2006Leo and Greene, 2008), by the finding of an implicit expression of hippocampus-dependent memory indexed by eye movements (Hannula and Ranganath, 2009;Voss et al, 2011), and by the finding of unconscious association formation and retrieval with concurrent hippocampal activation (Henke et al, 2003a,b;Degonda et al, 2005). Our current findings extend these previous findings by showing that the exclusion of conscious awareness of encoding and retrieval does not abolish rapid relational integration or long-term storage or the flexible expression of memories in new contexts or task-related hippocampal computation.…”

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

“…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).…”

“…Neurophysiological studies support the hypothesis that during VTE an animal is using its "cognitive map" by internally representing potential pathways (Johnson and Redish 2007) and evaluating future outcomes (van der Meer and Redish 2010). Various studies have shown that VTE is supported by the hippocampus (Hu and Amsel 1995;Voss et al 2011), occurs early in learning (Tolman 1939;van der Meer and Redish 2010), and increases with changes in task demands (Blumenthal et al 2011). However, to date, it has been difficult to determine the degree to which VTE behavior is linked to the different decisionmaking systems available.…”

“…Previous studies have shown that VTE is impaired in hippocampal amnesic humans (Voss et al 2011) and in rodents with hippocampal lesions (Hu and Amsel 1995), and is correlated with hippocampal activity (Hu et al 2006;Johnson and Redish 2007;Voss et al 2011). In the current study, VTE behaviors were seen on both hippocampal and nonhippocampal tasks: the Fixed Task, Novel Place Task, and Novel Response Task.…”

Human vicarious trial and error is predictive of spatial navigation performance

“…At the very least, the neuronal apparatus serving spatial representation has been found in the human hippocampus 10 . Also, at the behavioral level, human saccade-fixate-saccade sequences have been reported during moments of decision-making in visuospatial tasks, suggesting that humans also project onto their possible options before taking a decision 11,12 . Thus, one could expect that similar to rodents, specific behavioral mechanisms take place during the various stages of spatial learning in the human model.…”