Article

The role of the hippocampus in prediction and imagination.

Howard Hughes Medical Institute at Harvard University, Cambridge, Massachusetts 02138, USA.
Annual Review of Psychology (Impact Factor: 20.53). 01/2010; 61:27-48, C1-8. DOI: 10.1146/annurev.psych.60.110707.163508
Source: PubMed

ABSTRACT Traditionally, the hippocampal system has been studied in relation to the goal of retrieving memories about the past. Recent work in humans and rodents suggests that the hippocampal system may be better understood as a system that facilitates predictions about upcoming events. The hippocampus and associated cortical structures are active when people envision future events, and damage that includes the hippocampal region impairs this ability. In rats, hippocampal ensembles preplay and replay event sequences in the absence of overt behavior. If strung together in novel combinations, these sequences could provide the neural building blocks for simulating upcoming events during decision-making, planning, and when imagining novel scenarios. Moreover, in both humans and rodents, the hippocampal system is spontaneously active during task-free epochs and sleep, further suggesting that the system may use idle moments to derive new representations that set the context for future behaviors.

1 Follower
 · 
126 Views
  • Source
    [Show abstract] [Hide abstract]
    ABSTRACT: The capacity to adapt to resource distributions by modulating the frequency of exploratory and exploitative behaviors is common across metazoans and is arguably a principal selective force in the evolution of cognition. Here we (1) review recent work investigating behavioral and biological commonalities between external foraging in space and internal foraging over environments specified by cognitive representations, and (2) explore the implications of these commonalities for understanding the origins of the self. Behavioural commonalities include the capacity for what is known as area-restricted search in the ecological literature: this is search focussed around locations where resources have been found in the past, but moving away from locations where few resources are found, and capable of producing movement patterns mimicking Lévy flights. Area-restricted search shares a neural basis across metazoans, and these biological commonalities in vertebrates suggest an evolutionary homology between external and internal foraging. Internal foraging, and in particular a form we call embodied prospective foraging, makes available additional capacities for prediction based on search through a cognitive representation of the external environment, and allows predictions about outcomes of possible future actions. We demonstrate that cognitive systems that use embodied prospective foraging require a primitive sense of self, needed to distinguish actual from simulated action. This relationship has implications for understanding the evolution of autonoetic consciousness and self-awareness [Current Zoology 61 (2): 368–381, 2015]. While studying the abilities of rats to navigate mazes, Tolman and colleagues observed that in many cases rats took routes that suggested they could piece together memories in a way that allowed them to make novel inferences (Tolman, 1948; Tolman and Gleitman, 1949). As opposed to simple cue-response relationships that might be sufficient to learn a maze, the animals demonstrated the ability to make the kind of inferences that would require search over some form of internal repre-sentation—akin to realizing that one could go to India by taking a novel route around the earth. Tolman (1948) called these representations " cognitive maps " and argued that they provided a vast repertoire of behaviour not conceivable under the standard behaviorist's stimulus response theories. What is meant by a cognitive map and which species, if any, have them is highly debated (Cheung et al., 2014; Cruse and Wehner, 2011; Tsoar et al., 2011). For our purposes it is necessary only that these " maps " be cognitive representations of the world and involve a sense of place such that some things can be nearer to one another than others. The capacity to search through internal representations provides a means for working out how to get from one place to another. But it also allows another kind of behaviour—delibera-tion. That is, cognitive representations that can be internally searched should provide organisms with the capacity to explore alternatives, via internal foraging, prior to committing themselves to one course of action. Meunzinger and Fletcher (1938) called behavioural evidence consistent with internal foraging—that is, apparent deliberation at a choice point—vicarious trial-and-error and learning, and showed that it correlated with subsequent performance (see also Hu and Amsel, 1995). More recent evidence from neuroscience indicates that animals at choice points activate areas of the brain associated with the outcomes of past decisions at that point. One goal of this article is to provide a basis for understanding why this kind of internal foraging may have been pre-adapted for by the evolution of external foraging. A second goal is to explore the consequences of internal foraging for the existence of a precursor to self-awareness, or what Tulving (1985) called autonoetic consciousness: " Autonoetic (self-knowing) conscious
  • Source
    [Show abstract] [Hide abstract]
    ABSTRACT: Theories of brain function have evolved through multiple stages. The first proposition was that brain networks support a set of reflex responses, with current sensory inputs producing immediate motor outputs. The behaviorist paradigm suggested that actions can always be explained as a response to immediate external cues. In response to these views, the cognitive paradigm argued that behavior cannot be understood simply as input-output functions because the hidden layers of brain generate unpredictability. The central processing was termed "cognition." Here we propose a neuroscience-based model of cognition. Our core hypothesis is that cognition depends on internal models of the animal and its world, where internally generated sequences can serve to perform "what if" scenarios and anticipate the possible consequences of alternative actions without actually testing them, and aid in the decisions of overt actions. We support our hypotheses by several examples of recent experimental findings and show how externally guided cell assembly sequences become internalized to support cognitive functions. Copyright © 2014 Cold Spring Harbor Laboratory Press; all rights reserved.
    Cold Spring Harbor Symposia on Quantitative Biology 03/2015; DOI:10.1101/sqb.2014.79.024679
  • [Show abstract] [Hide abstract]
    ABSTRACT: It is widely agreed upon that linguistic predictions are an integral part of language comprehension. Yet, experimental proof of their existence remains challenging. Here, we introduce a new predictive eye gaze reading task combining eye-tracking and functional magnetic resonance imaging (fMRI) that allows us to infer the existence and timing of linguistic predictions via anticipatory eye-movements. Participants read different types of word sequences (i.e., regular sentences, meaningless jabberwocky sentences, non-word lists) up to the pre-final word. The final target word was displayed with a temporal delay and its screen position was dependent on the syntactic word category (nouns vs. verbs). During the delay, anticipatory eye-movements into the correct target word area were indicative of linguistic predictions. For fMRI analysis, the predictive sentence conditions were contrasted to the non-word condition, with the anticipatory eye-movements specifying differences in timing across conditions. A conjunction analysis of both sentence conditions revealed the neural substrate of word category prediction, namely a distributed network of cortical and subcortical brain regions including language systems, basal ganglia, thalamus, and hippocampus. Direct contrasts between regular sentence condition and jabberwocky condition indicate that prediction of word category in meaningless jabberwocky sentences relies on classical left-hemispheric language systems involving Brodman’s area 44/45 in the left inferior frontal gyrus, left superior temporal areas, and the dorsal caudate nucleus. Regular sentences, in contrast, allowed for the prediction of specific words. Word-specific predictions were specifically associated with more widely distributed temporal and parietal cortical systems, most prominently in the right hemisphere. Our results support the presence of linguistic predictions during sentence processing and demonstrate the validity of the predictive eye gaze paradigm for measuring syntactic and semantic aspects of linguistic predictions, as well as for investigating their neural substrates.
    Cortex 04/2015; DOI:10.1016/j.cortex.2015.04.011 · 6.04 Impact Factor