Hippocampal substrate of sensory associations

Port, Richard L.; Beggs, Alvin L.; Patterson, Michael M.

doi:10.1016/0031-9384(87)90167-3

Cited by 53 publications

(48 citation statements)

References 28 publications

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“…This result is consistent with the report by Port et al (1987), who showed that excitotoxic lesions to area CA1 of the hippocampus abolish sensory preconditioning within nictitating membrane response conditioning, and with Nicholson and Freeman (2000), who show that perirhinal cortex lesions abolish sensory preconditioning. One difference between the present and prior results, however, is that in the present study, large hippocampal lesions did not entirely abolish sensory preconditioning performance.…”

Section: Discussionsupporting

confidence: 93%

“…This flexibility of potential behavioral expression after sensory associations in sensory preconditioning is similar to transitive inference across paired associates, which has been considered to be analogous to a declarative memory process potentially dependent on an intact hippocampus (Bunsey and Eichenbaum, 1996;Honey et al, 1998). Indeed, studies have shown that lesions to the hippocampus and related structures within the medial temporal lobe block sensory preconditioning performance, using nictitating membrane conditioning (Port and Patterson, 1984;Port et al, 1987;Nicholson and Freeman, 2000). The current experiment further establishes that sensory preconditioning requires an intact hippocampal formation.…”

Section: Experiments 1: Hippocampal Basis For Sensory Preconditioningsupporting

confidence: 64%

“…For instance, rats can develop anticipatory orienting responses to the location of a light during light-predicting tone (Honey et al, 1998), and tone will elicit conditioned eyeblink responses when paired with a strong photic stimulus in eyeblink conditioning procedures (Rogers et al, 1999). This latter type of sensory-sensory behavioral conditioning could explain the result reported by Port et al (1987) that tone elicits larger hippocampal multi-unit responses when it predicts light onset during sensory preconditioning using the eyeblink paradigm. Sensory-sensory behavioral conditioning is of less concern here because both stimuli are within the same auditory modality and S2-anticipating orienting responses beyond that already produced by S1 are unlikely.…”

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confidence: 93%

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Hippocampal function during behaviorally silent associative learning: Dissociation of memory storage and expression

Talk

Gandhi

Matzel³

2002

Hippocampus

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ABSTRACT:In laboratory studies, the assessment of memory is typically associated with overt behavioral responses. Thus, it has been difficult to determine whether the enhancement of hippocampal sensoryevoked potentials that often accompany memory formation are the neurophysiological manifestation of a memory "trace" or are a secondary product of the behavioral expression of the memory. We addressed this issue by examining changes in evoked hippocampal field potentials during sensory preconditioning, a form of behaviorally silent relational learning that requires an intact hippocampus for execution. Rats were exposed to presentations of a white noise (S1) that terminated with a tone (S2). These pairings of ostensibly "neutral" stimuli supported no change in the behavior elicited by the noise. However, if the tone was subsequently paired with mild footshock (US), suppression of ongoing licking behavior (indicative of fear) was elicited by the noise, indicating that the animal had associated the noise with tone (S1-S2), and had represented the noisetone-shock (S1-S2-US) relationship. Pre-training neurotoxic lesions of the hippocampus had no effect on conditioned suppression to tone after tone-shock (S2-US) pairings, but disrupted the expression of continued suppression to noise (S1) after tone-shock pairings. In a second experiment, sensory-evoked field potentials in the dorsal hippocampus were recorded with extracellular electrodes. No changes in the hippocampal response evoked by white noise were observed after pairings of noise and tone, i.e., no evidence for a memory trace could be detected. In contrast, after tone was paired with footshock, two short-latency negative potentials within the noise-evoked field response increased in amplitude, a response often presumed to reflect a neurophysiological correlate of memory storage. In total, these results suggest that although the hippocampus critically contributes to the processing of a behaviorally silent associative memory, there may be no role for changes in the amplitude of hippocampal sensory-evoked field potentials in storing representations of the relationships between sensory experiences. Hippocampus 2002;12:648-656.

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Section: Discussionsupporting

confidence: 93%

Section: Experiments 1: Hippocampal Basis For Sensory Preconditioningsupporting

confidence: 64%

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confidence: 93%

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Hippocampal function during behaviorally silent associative learning: Dissociation of memory storage and expression

Talk

Gandhi

Matzel³

2002

Hippocampus

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“…The identification of the caudate nucleus as a structure mediating at least some of the learning that is spared following hippocampal damage allows for experiments that can assess these theories by manipulating both substrates. 1984: Port et al, 1987).…”

Section: Discussionmentioning

confidence: 99%

Differential effects of fornix and caudate nucleus lesions on two radial maze tasks: evidence for multiple memory systems

1989

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The present experiments were designed to examine the hypothesis that the mammalian brain contains anatomically distinct memory systems. Rats with bilateral lesions of caudate nucleus or fimbria-fornix and a control group were tested postoperatively on 1 of 2 versions of the radial maze task. In a standard win-shift version, each of the 8 arms of the maze was baited once, and the number of errors (revisits) in the first 8 choices of each trial was recorded. Fimbria-fornix rats were impaired in choice accuracy, while caudate animals were unimpaired relative to controls. Different groups of rats with similar lesions were tested on a newly developed win-stay version of the radial maze, in which the location of 4 randomly selected baited arms was signaled by a light at the entrance to each arm, and which required rats to revisit arms in which reinforcement had been previously acquired within a trial. Rats with fimbria-fornix lesions were superior to controls in choice accuracy on the win-stay radial maze task, while caudate animals were impaired relative to controls. The results demonstrate a double dissociation of the mnemonic functions of the hippocampus and caudate nucleus. Some implications of the presence of 2 memory systems in the mammalian brain are discussed.

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“…These investigations have revealed that the hippocampus and surrounding regions are important for SPC, as lesions to the hippocampus (Talk et al 2002), perirhinal cortex (Nicholson and Freeman 2000), CA1 (Port et al 1987), and surrounding fibers (Port and Patterson 1984) block the effects of SPC while leaving classical conditioning intact (Port and Patterson 1984;Port et al 1987). Associative learning models have implicated the hippocampal region as critical for several forms of conditioned learning that involve the representation of conditional stimuli (e.g., Gluck and Myers 1993;Schmajuk et al 1996).…”

Section: Conceptual Fear Generation Wwwlearnmemorgmentioning

confidence: 99%

Conceptual similarity promotes generalization of higher order fear learning

Dunsmoor¹,

White²,

LaBar³

2011

Learn. Mem.

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We tested the hypothesis that conceptual similarity promotes generalization of conditioned fear. Using a sensory preconditioning procedure, three groups of subjects learned an association between two cues that were conceptually similar, unrelated, or mismatched. Next, one of the cues was paired with a shock. The other cue was then reintroduced to test for fear generalization, as measured by the skin conductance response. Results showed enhanced fear generalization that correlated with trait anxiety levels in the group that learned an association between conceptually similar stimuli. These findings suggest that conceptual representations of conditional stimuli influence human fear learning processes.The idea that many fears originate from an association between neutral and aversive stimuli has continued to serve as the basis for influential accounts of human anxiety disorders (Bouton 2002;Mineka and Zinbarg 2006). However, the nexus of many fears defy a straightforward explanation, since following an aversive experience other stimuli that are indirectly related to the experience oftentimes become feared as well. In some cases, generalizing an acquired fear following an emotional learning episode is predicated on an association between stimuli formed before the emotional experience occurred. This form of stimulus generalization is known as sensory preconditioning (SPC) (Brogden 1939;Kimmel 1977;Gewirtz and Davis 2000), and is an important process whereby the representation of a known stimulus is modified following a salient experience with a related stimulus.A typical SPC procedure occurs in three phases: first, subjects learn to associate two neutral cues-for example, a bell and a light. Next, one of the cues, say the light, is associated with a biologically significant unconditioned stimulus (US), which leads to the development of a conditioned response (CR). The bell is called the preconditioned stimulus (PS) and the light is called the conditioned stimulus (CS). Finally, the PS is presented alone. Despite the fact that it has never predicted the US directly, the PS will often elicit a CR, suggesting that an association was formed during preconditioning between the PS and CS. The majority of SPC studies have been conducted in nonhuman animals (Brogden 1939;Rizley and Rescorla 1972). SPC effects have also been reported in a small number of human fear-conditioning experiments (White and Davey 1989;Vansteenwegen et al. 2000), but human research on this topic is very limited relative to experiments using first-order Pavlovian conditioning procedures. Consequently, the features that promote fear generalization between previously associated stimuli are unknown.A well-known factor important for classical conditioning (Rescorla and Furrow 1977) and stimulus generalization overall is similarity to the CS (Pavlov 1927;McLaren and Mackintosh 2002). Classic experiments of stimulus generalization in animals (reviewed in Honig and Urcuioli 1981) have revealed orderly generalization gradients of conditioned responses that tra...

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Hippocampal substrate of sensory associations

Cited by 53 publications

References 28 publications

Hippocampal function during behaviorally silent associative learning: Dissociation of memory storage and expression

Hippocampal function during behaviorally silent associative learning: Dissociation of memory storage and expression

Differential effects of fornix and caudate nucleus lesions on two radial maze tasks: evidence for multiple memory systems

Conceptual similarity promotes generalization of higher order fear learning

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