Anthony J. Greene

An fMRI Analysis of the Human Hippocampus: Inference, Context, and Task Awareness

The hippocampus is critical for encoding and retrieving semantic and episodic memories. Animal studies indicate that the hippocampus is also required for relational learning tasks. A prototypical relational learning task, and the one investigated in this experiment, using event-related functional magnetic resonance imaging, is the transitive inference (TI) task. In the TI task, participants were to choose between A and B (A?B) and learned by trial and error to choose A (A > B). There were four such premise pairs during a training (A > B, B > C, C > D, D > E). These can be acquired distinctly or can be organized into a superordinate hierarchy (A > B > C > D > E), which would efficiently represent all the learned relations and allow inferences (e.g., B > D). At test there was no reinforcement: In addition to premise pairs, untrained pairings were introduced (e.g., A?E, B?D). Correctly inferring that B > D is taken as evidence for the formation of a superordinate hierarchy; several alternatives to the superordinate hierarchy hypothesis are considered. Awareness of the formation of this hierarchy was measured by a postscan questionnaire. Four main findings are reported: (1) Inferential performance and task awareness dissociated behaviorally and at the level of hemodynamic response; (2) As expected, performance on the inferred relation, B > D, corresponded to the ability to simultaneously acquire B > C and C > D premise pairs during training; (3) Interestingly, acquiring these inner pairs corresponded to greater hippocampal activation than the outer pairs (A > B, D > E) for all participants. However, a distinct pattern of hippocampal activity for these inner pairs differentiated those able to perform the inferential discrimination, B > D, at test. Because these inner premise pairs require contextual discrimination (e.g., C is incorrect in the context of B but correct in the context of D), we argue that the TI task is hippocampal-dependent because the premise pair acquisition necessary for inference is hippocampal-dependent; (4) We found B > D related hippocampal activity at test that is anatomically consistent with preconsolidation recall effects shown in other studies.

Relational learning with and without awareness: Transitive inference using nonverbal stimuli in humans

Learning complex relationships among items and representing them flexibly have been shown to be highly similar in function and structure to conscious forms of learning. However, it is unclear whether conscious learning is essential for the exhibition of flexibility in learning. Successful performance on the transitive inference task requires representational flexibility. Participants learned four overlapping premise pairs (A > B, B > C, C > D, D > E) that could be encoded separately or as a sequential hierarchy (A > B > C > D > E). Some participants (informed) were told prior to training that the task required an inference made from premise pairs. Other participants (uninformed) were told simply that they were to learn a series of pairs by trial and error. Testing consisted of unreinforced trials that included the nonadjacent pair, B versus D, to assess capacity for transitive inference. Not surprisingly, those in the informed condition outperformed those in the uninformed condition. After completion of training and testing, uninformed participants were given a postexperimental questionnaire to assess awareness of the task structure. In contrast with expectations, successful performance on the transitive inference task for uninformed participants does not depend on or correlate with postexperimental awareness. The present results suggest that relational learning tasks do not necessarily require conscious processes.

The hippocampus reevaluated in unconscious learning and memory: at a tipping point?

Classic findings from the neuropsychological literature invariably indicated that performances on tests of memory that can be accomplished without conscious awareness were largely spared in amnesia, while those that required conscious retrieval (e.g., via recognition or recall) of information learned in the very same sessions was devastatingly impaired. Based on reports of such dissociations, it was proposed that one of the fundamental distinctions between memory systems is whether or not they support conscious access to remembered content. Only recently have we come to realize that the putative systemic division of labor between conscious and unconscious memory is not so clean. A primary goal of this review is to examine recent evidence that has been advanced against the view that the hippocampus is selectively critical for conscious memory. Along the way, consideration is given to criticisms that have been levied against these findings, potential explanations for differences in the reported results are proposed, and methodological pitfalls in investigations of unconscious memory are discussed. Ultimately, it is concluded that a tipping point has been reached, and that while conscious recollection depends critically on hippocampal integrity, the reach of the hippocampus extends to unconscious aspects of memory performance when relational memory processing and representation are required.

Visual–Auditory Events: Cross-Modal Perceptual Priming and Recognition Memory

Modality specificity in priming is taken as evidence for independent perceptual systems. However, Easton, Greene, and Srinivas (1997) showed that visual and haptic cross-modal priming is comparable in magnitude to within-modal priming. Where appropriate, perceptual systems might share like information. To test this, we assessed priming and recognition for visual and auditory events, within- and across- modalities. On the visual test, auditory study resulted in no priming. On the auditory priming test, visual study resulted in priming that was only marginally less than within-modal priming. The priming results show that visual study facilitates identification on both visual and auditory tests, but auditory study only facilitates performance on the auditory test. For both recognition tests, within-modal recognition exceeded cross-modal recognition. The results have two novel implications for the understanding of perceptual priming: First, we introduce visual and auditory priming for spatio-temporal events as a new priming paradigm chosen for its ecological validity and potential for information exchange. Second, we propose that the asymmetry of the cross-modal priming observed here may reflect the capacity of these perceptual modalities to provide cross-modal constraints on ambiguity. We argue that visual perception might inform and constrain auditory processing, while auditory perception corresponds to too many potential visual events to usefully inform and constrain visual perception.

Analogical inference: the role of awareness in abstract learning.

The acquisition and flexible expression of complex relations is often attributed to declarative memory processes. The extent to which such tasks may be done implicitly has not been sufficiently explored. We report that analogical or transfer processes may be accomplished implicitly. Our analogy task requires acquisition of a transverse patterning set, and then tests for transfer on an unrelated set. Participants learn the relations A>B (given a choice between A and B choose A) and B>C and the unrelated set X>Y and Y>Z. Only the experimental group was trained on the transverse pair C>A. At test all trials are unreinforced: A?B, B?C, A?C, X?Y, Y?Z, X?Z. Analogy was observed when the experimental group chose Z>X at greater frequency than controls who uniformly chose X>Z. Analogy occurred with or without awareness of the transfer. The capacity to transfer relations to an analogous set demonstrates a level of flexibility and abstraction not generally thought to be possible for implicit processes.

Is awareness necessary for true inference

In transitive inference, participants learn a set of context-dependent discriminations that can be organized into a hierarchy that supports inference. Several studies show that inference occurs with or without task awareness. However, some studies assert that without awareness, performance is attributable to pseudoinference. By this account, inference-like performance is achieved by differential stimulus weighting according to the stimuli’s proximity to the end items of the hierarchy. We implement an inference task that cannot be based on differential stimulus weighting. The design itself rules out pseudoinference strategies. Success on the task without evidence of deliberative strategies would therefore suggest that true inference can be achieved implicitly. We found that accurate performance on the inference task was not dependent on explicit awareness. The finding is consistent with a growing body of evidence that indicates that forms of learning and memory supporting inference and flexibility do not necessarily depend on task awareness.

A source of individual variation

Abstract Even though behavioral experiments are usually conducted in a manner that minimizes variance between subjects, such variance is unavoidable—even when working with a homogenous population. A first step in producing a quantitative understanding of what causes this variation is a biologically based neural network model that reproduces the observed individual differences. Here we show that a simple model of the hippocampus can reproduce the histogram of learned performance in a homogenous population. The task and data being fit is transitive inference that is learned by college students. Individual differences mainly arise from initial connectivity differences not neuronal state initializations.

Implicit analogy: New direct evidence and a challenge to the theory of memory

The authors propose that analogical reasoning may be achieved without conscious or explicit deliberation. The argument would be strengthened by more convincingly demonstrating instances of analogy that do not require explicit deliberation. Recent findings demonstrate that deliberative or explicit strategies are not necessary for flexible expression under novel circumstances (Greene et al. 2001) to include analogical transfer (Gross & Greene 2007). This issue is particularly critical because the existence of relational priming poses a serious challenge to the widely held notion that flexible expression of learned relations requires deliberative processes.

Individual differences: Variation by design

Anthony J. Greene & William B Levy University of Virginia Correspondence: Anthony Greene University of Virginia Department of Neurosurgery, HSC Box 420 Charlottesville, VA 22908 ajg3x@virginia.edu www.people.virginia.edu/~ajg3x 804.924.0356 Abstract: Stanovich & West appear to overlook the adaptivity of variation. Behavioral variability, both between and within individuals, is an absolute necessity for phylogenetic and ontological adaptation. As with all heritable characteristics, inter-individual behavioral variation is the foundation for natural selection. Similarly, intra-individual variation allows a broad exploration of potential solutions. Variation increases the likelihood that more optimal behaviors are available for selection. Four examples of the adaptivity of variation are discussed: a) Genetic variation as it pertains to behavior and natural selection; b) behavioral and cognitive aspects of mate selection which may facilitate genetic diversity; c) variation as a strategy for optimizing learning through greater exploration; and d) behavioral variation coupled with communication as a means to propagate individually discovered behavioral success.