Neuronal representations of stimulus associations develop in the temporal lobe during learning

Messinger, Adam; Squire, Larry R.; Zola, Stuart M.; Albright, Thomas D.

doi:10.1073/pnas.211431098

Cited by 156 publications

(154 citation statements)

References 40 publications

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“…Repeatedly viewing a pair of images close together in time is known to lead to pair coding in the ITC, as manifested in a tendency for neurons to respond with the same strength to both members of the pair (11,12,(15)(16)(17). It merits tangential note that we did observe pair coding, although pair coding was not the main focus of the study.…”

Section: Resultsmentioning

confidence: 55%

Statistical learning of visual transitions in monkey inferotemporal cortex

Meyer

Olson

2011

Proc. Natl. Acad. Sci. U.S.A.

270

271

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One of the most fundamental functions of the brain is to predict upcoming events on the basis of the recent past. A closely related function is to signal when a prediction has been violated. The identity of the brain regions that mediate these functions is not known. We set out to determine whether they are implemented at the level of single neurons in the visual system. We gave monkeys prolonged exposure to pairs of images presented in fixed sequence so that each leading image became a strong predictor for the corresponding trailing image. We then monitored the responses of neurons in the inferotemporal cortex to image sequences that obeyed or violated the transitional rules imposed during training. Inferotemporal neurons exhibited a transitional surprise effect, responding much more strongly to unpredicted transitions than to predicted transitions. Thus, neurons even in the visual system make experience-based predictions and react when they fail.macaque | vision | plasticity T he inferotemporal cortex (ITC), the terminus of the ventral stream of visual areas (1), plays a critical role in object vision (2, 3). ITC neurons respond with individual patterns of selectivity to complex images (4). Training monkeys to discriminate between images (5-7), categorize them (8, 9), or form associations between them (10-12) induces functional changes among neurons in the ITC which have the effect of strengthening the representation of image attributes relevant to task performance. Even passive viewing causes changes in neuronal visual responsiveness. Repeated viewing of a single image leads to a weakening of responses to it (13,14). Repeated viewing of two images close together in time leads to pair coding: a tendency for neurons responsive to one image also to respond to the other (15-17). The effects of passive viewing, because they do not depend on task demands, fall into the category of unsupervised statistical learning.An important form of unsupervised learning not previously studied at the level of single neurons concerns transitional statistics. The learning of transitional statistics has been the focus of much behavioral study in humans because it is thought to underlie the development during infancy of the ability to perceive event boundaries including word boundaries in speech (18,19). Human infants passively exposed to a stimulus stream in which certain visual images always follow certain others automatically register the transitional rules as evidenced by their orienting preferentially to a test stream containing novel transitions (20). The adult human brain is sensitive to transitional probabilities, as evidenced by its generating strong responses to improbable transitions at the level of scalp potential and blood oxygenation measures (21-27). Monkeys, like human infants, have been reported to learn transitional probabilities and to orient preferentially to improbable transitions (28). No effort has been made as yet to characterize the underlying neuronal mechanisms (29). We hypothesized that neurons in the ITC ...

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Section: Resultsmentioning

confidence: 55%

Statistical learning of visual transitions in monkey inferotemporal cortex

Meyer

Olson

2011

Proc. Natl. Acad. Sci. U.S.A.

270

271

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“…9). There is considerable evidence for just this phenomenon in the primate (Higuchi & Miyashita, 1996;Messinger et al, 2001;Miyashita, 1988;Naya et al, 2001). …”

Section: Discussionmentioning

confidence: 99%

The Temporal Context Model in Spatial Navigation and Relational Learning: Toward a Common Explanation of Medial Temporal Lobe Function Across Domains.

Howard¹,

Fotedar²,

Datey³

et al. 2005

Psychological Review

271

334

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The medial temporal lobe (MTL) has been studied extensively at all levels of analysis, yet its function remains unclear. Theory regarding the cognitive function of the MTL has centered along 3 themes. Different authors have emphasized the role of the MTL in episodic recall, spatial navigation, or relational memory. Starting with the temporal context model (M. W. Howard and M. J. , a distributed memory model that has been applied to benchmark data from episodic recall tasks, the authors propose that the entorhinal cortex supports a gradually changing representation of temporal context and the hippocampus proper enables retrieval of these contextual states. Simulation studies show this hypothesis explains the firing of place cells in the entorhinal cortex and the behavioral effects of hippocampal lesion in relational memory tasks. These results constitute a first step towards a unified computational theory of MTL function that integrates neurophysiological, neuropsychological and cognitive findings.The medial temporal lobe (MTL) is a region that includes the hippocampus proper, the subicular complex and parahippocampal cortical regions, including entorhinal, perirhinal, and parahippocampal/postrhinal cortices. A great deal of data from neuropsychology (e.g. Eichenbaum & Cohen, 2001;Scoville & Milner, 1957;Squire, 1992) and functional imaging (e.g. Fernandez, Effern, Grunwald, et al., 1999;Stern, Corkin, Gonzalez, et al., 1996;Wagner et al., 1998) has converged on the idea that the MTL is important in learning and memory. In order to bridge the gap between cognition and cellular-level physiology, we need a mechanistic, mesoscopic description of MTL computational function. We already have several successful verbally-formulated theories of the cognitive function of the MTL. These are described in turn in the following subsections. This paper will attempt to draw these multiple verbal theories together into a single computational framework that is consistent with known neurophysiological and neuroanatomical data.

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“…A subsequent combined lesion and electrophysiology study further showed that the response of the IT neurons was dependent on the MTL, suggesting the interaction between the MTL and the IT neurons during formation of memory representation (Higuchi and Miyashita, 1996;Messinger et al, 2001). Whereas the role of the hippocampus in long-term memory formation in humans have also been investigated using noninvasive neuroimaging techniques (Stark and Squire, 2000;Haist et al, 2001;Takashima et al, 2006;Smith and Squire, 2009), the neocortical stores for more enduring memory representation largely remain to be explored.…”

Section: Introductionmentioning

confidence: 99%

Formation of Long-Term Memory Representation in Human Temporal Cortex Related to Pictorial Paired Associates

Yamashita¹,

Hirose²,

Kunimatsu³

et al. 2009

J. Neurosci.

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It is widely held that long-term memory gradually develops in the temporal neocortex after initial memory encoding into the hippocampus. However, little is known as to whether and where long-term memory can be newly created in the human temporal neocortex. In this functional magnetic resonance imaging study, we detected brain activity in the temporal neocortex that was developed ϳ8 weeks after study of unfamiliar pictorial paired associates. Two sets of paired Fourier figures were studied, one ϳ8 weeks before test and the other immediately before test, keeping the correct performance during the tests balanced across the two sets of stimuli. Significant signal increase was observed in the right hippocampus during retrieval of newly studied pairs relative to initially studied pairs. In contrast, significant signal increase was observed in the anterior temporal cortex during retrieval of initially studied pairs relative to newly studied pairs. The greater activity during retrieval of older memory developed in the temporal neocortex provides direct evidence of formation of temporal neocortical representation for stable long-term memory.

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Neuronal representations of stimulus associations develop in the temporal lobe during learning

Cited by 156 publications

References 40 publications

Statistical learning of visual transitions in monkey inferotemporal cortex

Statistical learning of visual transitions in monkey inferotemporal cortex

The Temporal Context Model in Spatial Navigation and Relational Learning: Toward a Common Explanation of Medial Temporal Lobe Function Across Domains.

Formation of Long-Term Memory Representation in Human Temporal Cortex Related to Pictorial Paired Associates

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