Exploration-dependent modulation of evoked responses in fascia dentata: dissociation of motor, EEG, and sensory factors and evidence for a synaptic efficacy change

Green, EJ; McNaughton, B. L.; Barnes, C. A.

doi:10.1523/jneurosci.10-05-01455.1990

Cited by 78 publications

(52 citation statements)

References 28 publications

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“…Indeed, the short DH context involvement duration throws doubt on the hypothesis that DH is necessary for context representation storage, in accord with previous statements (Otto et al, 1997). On this point, we may also recall that, in rats, a modification of electrical hippocampal activity (EPSP, population spike) was observed after exposure to new surroundings; the modification began during training and disappeared after 1 or 2 hr (Green et al, 1990). On the other hand, electrophysiological results obtained both in vitro (McKernan and Shinnick-Gallagher, 1997) and in vivo (Rogan et al, 1997) have shown that, after acquisition, there are in the BL A long-lasting modifications of electrical activity believed to be related to CS-US coupling.…”

Section: Discussionsupporting

confidence: 79%

Auditory Thalamus, Dorsal Hippocampus, Basolateral Amygdala, and Perirhinal Cortex Role in the Consolidation of Conditioned Freezing to Context and to Acoustic Conditioned Stimulus in the Rat

Sacchetti¹,

Lorenzini²,

Baldi³

et al. 1999

J. Neurosci.

222

221

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On the basis of previous experimental evidence, it is known that the auditory thalamus (AT), the dorsal hippocampus (DH), the basolateral amygdala (BLA), and the perirhinal cortex (PC) are involved in the mnemonic processing of conditioned freezing. In particular, BLA and PC appear to be involved both in conditioned stimulus (CS) and context conditioned freezing. Through AT, the auditory CS is sent to other sites, whereas DH is involved in context conditioning. Nevertheless, the existing evidence does not make it possible to assess AT, DH, BLA, and PC involvement during the consolidation phase of conditioned freezing. To address this question, fully reversible tetrodotoxin (TTX) inactivation was performed on adult male Wistar rats having undergone CS and context fear training. Anesthetized animals were injected stereotaxically with TTX (either 5 or 10 ng in 0.5 or 1.0 l of saline, according to site dimensions) at increasing post-acquisition delays. Context and CS freezing durations were measured during retention testing, always performed 48 and 72 hr after TTX administration. The results showed that AT inactivation does not disrupt consolidation of either contextual or auditory fear memories. In contrast, inactivation of the other three structures disrupted consolidation. For the DH, this disruption was specific to contextual cues and only occurred when inactivation was performed early (up to 1.5 hr) after training. The BLA and PC were shown to be involved in the consolidation of both contextual and auditory fear. Their involvement persisted for longer periods of time (2 d for BLA and 8 d for PC). These findings provide information to build a temporal profile for the post-training processing of fear memories in structures known to be important for this form of learning. The results are discussed in relation to previous studies on conditioned freezing and other aversive conditioned response neural correlates.

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Section: Discussionsupporting

confidence: 79%

Auditory Thalamus, Dorsal Hippocampus, Basolateral Amygdala, and Perirhinal Cortex Role in the Consolidation of Conditioned Freezing to Context and to Acoustic Conditioned Stimulus in the Rat

Sacchetti¹,

Lorenzini²,

Baldi³

et al. 1999

J. Neurosci.

222

221

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“…Nonetheless, the facts connecting the hippocampus to exploration, which play a central role in cognitive map theory, remain to be explained by any successful theory that seeks a more abstract characterization of hippocampal function. The recent demonstration of "exploration-dependent modulation" of evoked activity in the dentate gyrus (Sharp et al, 1989: Green et al, 1990 only confirms the importance of this connection between exploratory behavior and the hippocampal information-storage system.…”

Section: The Hippocampus As a Spatial Memory Systemmentioning

confidence: 99%

The hippocampus and space revisited

1991

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The hippocampal formation has long been the focus of intense interest among neuroscientists. The discovery by Scoville and Milner (1957) that the mesial temporal lobe, including the hippocampal formation, played a central role in memory function in humans can be said to have started the modern era of research on this brain system. There followed two decades of animal research aimed at creating experimental models of the memory defects observed in humans, including my dissertation research, which met with scant success (Nadel, 1968). Indeed, when John O'Keefe and I started considering the hippocampus and its possible role in spatial mapping several years later, one of our greatest challenges was to analyze the extant lesion literature in terms of this theory with the minimum amount of special pleading. There were already several hundred such studies, varying extensively in terms of exact size and regional location of the lesion, the means by which the lesion had been created, the kind of animal used, the nature of the task, the kind of motivation employed, and so on. Yet, it was our feeling in 1976, when we terminated the review of the lesion literature, which was ultimately published in The Hippocumpiis CIS a Cognitive Map (O'Keefe and Nadel, 1978), that the spatial hypothesis successfully handled the vast preponderance of these lesion studies as well as what was then known about the physiology of the hippocampal formation.In the years following publication of the book, most published lesion studies were concerned in some way with the spatial map hypothesis; most often, comparisons with rival hypotheses were involved. This was a frustrating period because, although many thought they were testing our ideas, too frequently the major themes we hoped to stress were misconstrued. In this article I dig back into the book we published in 1978 and reiterate some of the themes that were important to us then, and remain so now. By so doing, 1 hope to bring out some of the reasons why we thought, and continue to think, that space is so special as to warrant a structure as compelling as the hippocampal formation.I will concentrate on three major issues. First, I will discuss at some length the fact that our theory was about a ~p a t i a l memory system, not simply a "spatial" system. Second, Iwill discuss our assumption that the spatial memory system we allocated to the hippocampus was but one of many spatial systems, and that the role of these various systems can best be understood if one takes into consideration an animal's behavior in its natural habitat. Third, I will briefly discuss our view that in the human hippocampus, at least in the left hemisphere, the mapping system represents something more abstract than physical space.Before turning to these substantive points, however, a brief digression into methods and first principles is in order. Some years before the book was published, O'Keefe and I published a paper (Nadel and O'Keefe, 1974) in which we presented some of the reasons for hypothesizing that the hippocamp...

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“…Particularly interesting in light of the frequency dependence of the present results (Fig. 2) is the reported shift in the peak of the EEG power spectrum from 1 to 7 Hz as rats go from a state of stillness to active exploration of their environment (23).…”

Section: Discussionmentioning

confidence: 53%

Homosynaptic Long-Term Depression in Area CA1 of Hippocampus and Effects ofN-Methyl-D-Aspartate Receptor Blockade

Cooper¹

1995

How We Learn; How We Remember: Toward an Understanding of Brain and Neural Systems

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We tested a theoretical prediction that patterns ofexcitatory input activity that consistently fail to activate target neurons sufficiently to induce synaptic potentiation will instead cause a specific synaptic depression. To realize this situation experimentally, the Schaffer collateral projection to area CAl in rat hippocampal slices was stimulated electrically at frequencies ranging from 0.5 to 50 Hz. Nine hundred pulses at 1-3 Hz consistently yielded a depression of the CAl population excitatory postsynaptic potential that persisted without signs of recovery for >1 hr after cessation of the conditioning stimulation. This long-term depression was specific to the conditioned input, ruling out generalized changes in postsynaptic responsiveness or excitability. Three lines of evidence suggest that this effect is accounted for by a modification of synaptic effectiveness rather than damage to or fatigue of the stimulated inputs. First, the effect was dependent on the stimulation frequency; 900 pulses at 10 Hz caused no lasting change, and at 50 Hz a synaptic potentiation was usually observed. Second, the depressed synapses continued to support long-term potentiation in response to a high-frequency tetanus.Third, the effects of conditioning stimulation could be prevented by application of NMDA receptor antagonists. Thus, our data suggest that synaptic depression can be triggered by prolonged NMDA receptor activation that is below the threshold for inducing synaptic potentiation. We propose that this mechanism is important for the modifications of hippocampal response properties that underlie some forms of learning and memory.A cardinal feature of neuronal responses in the central nervous system is stimulus selectivity. Work on a number of preparations, including the developing visual cortex (1), adult somatosensory cortex (2), and hippocampus (3), has shown convincingly that neuronal selectivity can be modified by experience. It is a widely held belief that such modifications are a likely basis for learning and memory in mammals.Experience-dependent shifts in selectivity require that neurons acquire responsiveness to new stimuli and lose responsiveness to previously effective stimuli. A critical question concerns the mechanisms whereby this is accomplished. According to a theory developed for visual cortex (4-6), stimulus selectivity will evolve if excitatory synaptic inputs are potentiated when they consistently yield postsynaptic responses greater than a critical value (called the modification threshold, Om) and are depressed when they consistently yield responses greater than zero (the average "spontaneous" value) but less than 0m. Because the value of the modification threshold is a function of the average postsynaptic cell activity (5, 6), the selectivity ofa neuron can be modified when the probability of different patterns ofinput activity shifts, as it would when the animal is experiencing a novel environment.On the basis of work done on long-term potentiation (LTP) in area CA1 of the hippocampus (7)...

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Exploration-dependent modulation of evoked responses in fascia dentata: dissociation of motor, EEG, and sensory factors and evidence for a synaptic efficacy change

Cited by 78 publications

References 28 publications

Auditory Thalamus, Dorsal Hippocampus, Basolateral Amygdala, and Perirhinal Cortex Role in the Consolidation of Conditioned Freezing to Context and to Acoustic Conditioned Stimulus in the Rat

Auditory Thalamus, Dorsal Hippocampus, Basolateral Amygdala, and Perirhinal Cortex Role in the Consolidation of Conditioned Freezing to Context and to Acoustic Conditioned Stimulus in the Rat

The hippocampus and space revisited

Homosynaptic Long-Term Depression in Area CA1 of Hippocampus and Effects ofN-Methyl-D-Aspartate Receptor Blockade

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