Contextual cueing is not flexible.

Target detection is faster when search displays repeat, but properties of the memory representations that give rise to this contextual cueing effect remain uncertain. We adapted the contextual cueing task using an ABA design and recorded the eye movements of healthy young adults to determine whether the memory representations are flexible. Targets moved to a new location during the B phase and then returned to their original locations (second A phase). Contextual cueing effects in the first A phase were reinstated immediately in the second A phase, and response time costs eventually gave way to a repeated search advantage in the B phase, suggesting that two target-context associations were learned. However, this apparent flexibility disappeared when eye tracking data were used to subdivide repeated displays based on B-phase viewing of the original target quadrant. Therefore, memory representations acquired in the contextual cueing task resist change and are not flexible.

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.

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.

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.

Implicit transitive inference and the human hippocampus: does intravenous midazolam function as a reversible hippocampal lesion?

Recent advances have led to an understanding that the hippocampus is involved more broadly than explicit or declarative memory alone. Tasks which involve the acquisition of complex associations involve the hippocampus whether the learning is explicit or implicit. One hippocampal-dependent implicit task is transitive inference (TI). Recently it was suggested that implicit transitive inference does not depend upon the hippocampus (Frank, M. J., O'Reilly, R. C., & Curran, T. 2006. When memory fails, intuition reigns: midazolam enhances implicit inference in humans. Psychological Science, 17, 700-707). The authors demonstrated that intravenous midazolam, which is thought to inactivate the hippocampus, may enhance TI performance. Three critical assumptions are required but not met: 1) that deactivations of other regions could not account for the effect 2) that intravenous midazolam does indeed deactivate the hippocampus and 3) that midazolam influences explicit but not implicit memory. Each of these assumptions is seriously flawed. Consequently, the suggestion that implicit TI does not depend upon the hippocampus is unfounded.

Hippocampal differentiation without recognition: an fMRI analysis of the contextual cueing task.

A central role of the hippocampus is to consolidate conscious forms of learning and memory, while performance on implicit tasks appears to depend upon other structures. Recently, considerable debate has emerged about whether hippocampal-dependent tasks necessarily entail task awareness. In the contextual cueing task, repetition facilitation is implicit, but impaired in patients with amnesia. Whether the hippocampus alone or other MTL structures are required is unclear. Event-related functional magnetic resonance imaging revealed hippocampal activity that differentiates novel from repeated arrays. This pattern of results was observed without recognition of the repeating arrays. This finding provides support for the claim that the hippocampus is involved in processes outside the domain of conscious learning and memory.

Human hippocampal-dependent tasks: is awareness necessary or sufficient?

The hippocampus has been shown to be required for the acquisition of declarative or explicit memory. Whether all hippocampal-dependent forms of learning and memory are explicit is an open question. Controversy has emerged about the existence of implicit hippocampal-dependent tasks. Two implicit tasks that may involve the hippocampusare a relational eye tracking task (Ryan et al. (2000) Psychol Sci 11:454-461) and transitive inference (Greene et al. (2006) J Cognit Neurosci 18:1156-1173; Greene et al. (2001) Mem Cognit 29:893-902). Recently, it was shown that both of these tasks may depend upon task awareness (Smith et al. (2006) J Neurosci 26:11304-11312; Smith and Squire (2005) J Neurosci 25:10138-10146). It is argued that in both cases, distinct, explicit versions of the tasks were created, which do not disprove the implicit nature of the original tasks.

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.