The hippocampus and memory for orderly stimulus relations.

By Jeffery A. Dusek, Howard Eichenbaum. 1997

Human declarative memory involves a systematic organization of information that supports generalizations and inferences from acquired knowledge. This kind of memory depends on the hippocampal region in humans, but the extent to which animals also have declarative memory, and whether inferential expression of memory depends on the hippocampus in animals, remains a major challenge in cognitive neuroscience. To examine these issues, we used a test of transitive inference pioneered by Piaget to assess capacities for systematic organization of knowledge and logical inference in children. In our adaptation of the test, rats were trained on a set of four overlapping odor discrimination problems that could be encoded either separately or as a single representation of orderly relations among the odor stimuli. Normal rats learned the problems and demonstrated the relational memory organization through appropriate transitive inferences about items not presented together during training. By contrast, after disconnection of the hippocampus from either its cortical or subcortical pathway, rats succeeded in acquiring the separate discrimination problems but did not demonstrate transitive inference, indicating that they had failed to develop or could not inferentially express the orderly organization of the stimulus elements. These findings strongly support the view that the hippocampus mediates a general declarative memory capacity in animals, as it does in humans.

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Citations in the corpus

Generalization Through the Recurrent Interaction of Episodic Memories (2012, background): “D inference pair (Dusek & Eichenbaum, 1997).”
Hippocampal Amnesia Impairs All Manner of Relational Memory (2008, background): “…inference and transverse patterning performance, requiring hierarchical or other (non-spatial) relational representations among pairs of odors (Dusek and Eichenbaum, 1997, 1998), and memory for sequences of odors (Fortin et al., 2002); while hippocampal neuronal fi ring has been shown to…”
The temporal context model in spatial navigation and relational learning: toward a common explanation of medial temporal lobe function across domains. (2005, methodology): “Transitive associations and relational memory Data from olfactory learning in the rat (Bunsey & Eichenbaum, 1996; Dusek & Eichenbaum, 1997) has been used to argue that the hippocampus, the central structure of the MTL, enables transitive associations, a function believed to be important in…”
Dynamic Analysis of Learning in Behavioral Experiments (2004, background): “…of an animal to learn a new task is commonly tested to study how brain lesions (Whishaw and Tomie, 1991; Roman et al., 1993; Dias et al., 1997; Dusek and Eichenbaum, 1997; Wise and Murray, 1999; Fox et al., 2003), attentional modulation (Cook and Maunsell, 2002), genetic manipulations…”
Conjunctive representations in learning and memory: principles of cortical and hippocampal function. (2001, methodology): “This simulates the blocked training used by Dusek and Eichenbaum (1997), except that they used successively fewer trials per block in their repetitions.”
Transitivity, flexibility, conjunctive representations, and the hippocampus. I. An empirical analysis (2003, methodology): “We used training procedures very similar to those used by Dusek and Eichenbaum (1997) and replicated their results in all essential details. Most importantly, rats in the present experiment displayed transitive inference-like behavior. They responded by choosing B on the first trial of the BD test (”
Entorhinal Cortex Lesions Disrupt the Relational Organization of Memory in Monkeys (2004, background): “…to make inferential judgments about the relationships between familiar items presented in novel combinations and poor performance on previously acquired discriminations when items are presented in reverse of their original training order (Bunsey and Eichenbaum, 1996; Dusek and Eichenbaum, 1997).”
The hippocampus and inferential reasoning: building memories to navigate future decisions (2012, methodology): “In a series of animal lesion studies, Eichenbaum and colleagues trained rats on overlapping odor– odor associations using the associative inference (Bunsey and Eichenbaum, 1996) and transitive inference paradigms (Dusek and Eichenbaum, 1997).”
Generalization of value in reinforcement learning by humans (2012, background): “Consistent with the hypothesized role for the hippocampus in this generalization, functional connectivity between the ventral striatum and hippocampus was modulated, across participants, by the ability of the augmented model to capture participants’ choice.”
An investigation of learning strategy supporting transitive inference performance in humans compared to other species. (2006, background): “This was taken as evidence that the lesion rats were lacking inferential ability, suggesting that this ability is mediated by the hippocampal system (Dusek & Eichenbaum, 1997).”
Hippocampal activation during transitive inference in humans (2004, background): “Thus, this study confirms in humans the importance of the hippocampus for the orderly organization of stimulus relations, a finding previously demonstrated in rodents (Dusek and Eichenbaum, 1997; Van Elzakker et al., 2003), and extends recent fMRI studies of relational memory in humans (Rombouts et ”
The Tolman-Eichenbaum Machine: Unifying Space and Relational Memory through Generalization in the Hippocampal Formation (2019, background): “transitive inference problems (which depend on the hippocampus [Bunsey and Eichenbaum, 1996; Dusek and Eichenbaum, 1997]) require stimuli to be represented on an abstract ordered line, such that A>B and B>C implies A>C.”
Ask Me Anything: Dynamic Memory Networks for Natural Language Processing (2015, background): “Interestingly, it also appears that the hippocampus is active during transitive inference [30], and disruption of the hippocampus impairs this ability [31].”
The Episodic Memory System: Neurocircuitry and Disorders (2009, unknown): “Transitive inference, the ability to use previously learned associative relationships between items to draw inferences about probable associations that have never been specifically learned, seems to depend on the hippocampal formation (Dusek and Eichenbaum, 1997).”
Hippocampal Contributions to Model-Based Planning and Spatial Memory (2019, unknown): “Tests of relational encoding have even relied on tasks that are similar in logic to probes for model-based planning, like transitive inference or acquired equivalence (Dusek and Eichenbaum, 1997; Heckers et al., 2004; Shohamy and Wagner, 2008; Wimmer and Shohamy, 2012).”
Brain Mechanisms of Concept Learning (2019, methodology): “…learning (Kumaran et al., 2009; Bowman and Zeithamova, 2018; Frank et al., 2019) have been implicated in memory integration and inference in both neuroimaging (Zeithamova et al., 2012; Schlichting et al., 2015) and lesion work (Dusek and Eichenbaum, 1997; Ryan et al., 2016; Spalding et al., 2018).”