Phillip J. Best

Spatial correlates of hippocampal unit activity are altered by lesions of the fornix and entorhinal cortex

Behavioral and electrophysiological evidence supports the role of the hippocampus in the processing of spatial information. In the present study, neuronal activity recorded from chronically implanted hippocampal microelectrodes was correlated with a rats spatial orientation while traversing a radial maze for food reward. Place units were found in all fields of the dorsal hippocampus and dentate gyrus. Rotation of the maze relative to extramaze cues failed to disrupt the intact animals spatial task performance of the spatial correlates of the unit activity. Lesions of the fornix or entorhinal cortex disrupted performance of the task. Unit activity correlated to the animals spatial orientation was also disrupted by either lesion. There was no correlation between the disruption of the unit activity and location of the unit within hippocampal fields. Unit activity from lesioned animals showed correlation to the physical properties of the maze rather than to the orientation of the maze in space. These results further support the role of the hippocampus in the processing of spatial information.

Effects of deafness and blindness on the spatial correlates of hippocampal unit activity in the rat

Abstract Hippocampal cellular activity is closely related to a rats position in a test environment, such as a radial arm maze. After maze rotation, the cellular activity in intact rats shows persistence with respect to the extramaze environmental cues. The present study investigated the persistence of hippocampal spatial cells in deaf and blind rats. The fields of 11 of 15 spatial cells followed the local maze cues after maze rotation, similar to the fields previously seen in rats with entorhinal lesions. The fields of the other 4 cells persisted in their initial spatial locations. Spinning the rats disrupted directional persistence in 3 of the 4 cells, suggesting a possible role for vestibular cues in spatial firing. The blind-deaf rats were not significantly impaired in their behavioral performance on the 6-arm maze or on a 17-arm maze. Sensory deprivation had the same effect as entorhinal lesions on spatial firing but not on maze performance.

The Effects of State of Consciousness and Latent Inhibition on Hippocampal Unit Activity in the Rat during Conditioning

Abstract The activity of single cells in rat hippocampus was monitored in animals given 15 to 20 nonreinforced tone presentations prior to the administration of tone-shock pairings and in rats receiving no tone preexposure prior to aversive training. Tones were presented during both slow wave sleep and quiet waking. A reduction in hippocampal activity was seen to tones presented to the sleeping animal in the preexposed group. In addition, tones presented to waking animals enhanced activity in cells from the nonpreexposed group while having little effect on those in the preexposed group. Results are discussed in terms of attentional and stimulus salience models of hippocampal function.

Hippocampal unit activity to tonal stimuli during arousal from sleep and in awake rats

Abstract Single cell activity was recorded from electrodes chronically implanted in fascia dentata and the CA-1 field of dorsal hippocampus in unrestrained rats during presentations of tonal stimuli. In the first experiment 32% of the cells showed reliable decreases in activity to the tonal stimuli and 26% showed reliable increases. Most of these cells (73%) habituated under rapid tone presentation. The second experiment showed that tonal stimuli caused changes in activity in more cells when the tones aroused the animal from sleep (75% affected) than when the tone was presented to an awake animal (18% affected). In both experiments all affected fascia dentata cells were inhibited. However, 36% of the affected CA-1 cells were augmented. The data indicate that the hippocampus undergoes dramatic changes during arousal from sleep, and that previously found changes in hippocampal activity during conditioning might be due to conditioned changes in the capability of stimuli to arouse the animal from sleep.

Effects of hippocampal lesions on passive avoidance and taste aversion conditioning

Abstract Rats with electrolytic lesions of the posteroventral hippocampus failed to perform a simple passive avoidance of footshock but showed conditioned aversion to a saccharin solution paired with apomorphine induced gastrointestinal distress. On the other hand, anterodorsal hippocampal lesions interfered with performance on both tasks. The more general deficit produced by the dorsal lesions is attributed to the fact that such lesions extended into the fimbria, and thus destroyed outputs from a larger area of the hippocampus.

Mediodorsal thalamic lesions impair radial maze performance in the rat.

The role of the mediodorsal thalamic nucleus (MD) in spatial memory processes was assessed. Animals were preoperatively trained on an 8-arm maze placed in a visually deprived environment. Following 50 acquisition trials, one group received bilateral electrolytic lesion of the MD thalamus, whereas the other group received sham lesions. On postoperative tests of radial maze performance, MD lesioned animals made significantly more errors, made more errors sooner, and emitted fewer correct responses before making an error than did sham controls. The lesioned subjects also exhibited considerable perseveration immediately postoperation and developed response patterning on postlesion trials. Lesions of the mediodorsal thalamus may fundamentally compromise memory systems and alter ability to respond appropriately in a minimally cued environment.

Neural activity in the dorsal hippocampus during paradoxical sleep, slow wave sleep and waking

Abstract Dorsal hippocampal single cell activity was recorded from chronically implanted electrodes in unrestrained rats during naturally occurring episodes of quiet waking, sleep with slow waves and paradoxical sleep. A clear differentiation of cellular activity is seen between those areas of Cajals regio superior, regio inferior and fascia dentata. During paradoxical sleep the regio superior shows its lowest level of activity, while regio inferior and fascia dentata show their highest levels. It is suggested that apparent discrepancies between previous studies of hippocampal activity during paradoxical sleep might be due to differences in recording site. The data also imply the existence of a previously undescribed inhibitory pathway, probably via the fimbria, which is differentially active during paradoxical sleep.

Drug-preexposure effects in flavor-aversion learning: Associative interference by conditioned environmental stimuli.

Previous research has documented that exposure to a drug reduces the ability of the drug to support subsequent flavor-aversion learning. The four experiments reported here examined the hypothesis that this drug-preexposure effect is due to associative interference from environmental stimuli associated with the drug effects during preexposure. When distinctive environmental stimuli (confinement in a black compartment) were present during drug preexposure, these stimuli significantly disrupted subsequent flavor-aversion learning. Furthermore, flavor conditioning was not significantly disrupted when drug preexposure occurred in the absence of salient environmental stimuli or when the previously conditioned environmental stimuli were extinguished prior to flavor conditioning. It is significant, and in contrast to other published research, that flavor conditioning was not disrupted when the distinctive cues paired with the drug during preexposure were absent at the time of the flavor-drug pairing. These results are thus consistent with results from conventional studies of stimulus blocking and suggest that associative processes can play a major role in the drug-preexposure effect.

Reliability of the relationship between hippocampal unit activity and sensory-behavioral events in the rat

The relationship of hippocampal cellular activity to behavior was assessed by making videotapes of recording sessions which sampled a variety of behaviors in the rat. The unit signals were displayed via a split screen device on the upper one-quarter of the picture. The output of a unit discriminator was presented on the audio channel of the tape. The tapes were later presented to naive observers who kept a running account of the behaviors correlated with fast or slow cell activity. The observers were also instructed to draw conclusions about the relationship between each cells activity and behavior, and to state their confidence level in their conclusions. Twenty-three tapes were made, 14 hippocampal complex spike cells, 5 theta cells, one thalamic cell, and 3 control tapes in which complex spike activity from one session was presented with behaviors of another session. The observers showed high confidence and strong agreement on most of the cells. Of the 15 complex spike cells, 9 were judged to be related to the animals position in space, 2 were related to turning movement, and 1 to drinking. The 5 theta cells were all related to general movement. The students found no compelling sensory behavioral correlates for 2 complex spike cells, the thalamic cell, and the 3 control tapes. The results indicate that hippocampal cellular activity is much more related to an animals position in space than to the variety of sensory behavioral events previously described by J. Ranck (1973, Exp. Neurol.41: 461–531). The study also shows that a high degree of reliability can be obtained in the observational approach by the presentation of tapes of behavior to a large number of observers.

Response biases do not underlie the radial maze deficit in rats with mediodorsal thalamus lesions

Previous results indicating that radial maze performance in animals with mediodorsal thalamic lesions is deficient cannot exclude the possibility that these impairments are due to altered motor mechanisms (response biases). The present study sought to eliminate this potentially confounding variable by using a procedure which tests memory for serial position. This procedure involved experimenter-controlled arm entry (number and order) on a radial arm maze. Following this sequence, animals were presented with one previously entered arm along with an arm not yet visited on that trial. Avoidance of the previously entered arm constituted memory for the prior sequence. Thus, this task represents a form of a win-shift or nonmatching-to-sample task. Seven animals were given ibotenic acid lesions of the mediodorsal nucleus and nine others were given sham operations; 2 weeks later testing in the above procedure was conducted. Results indicated that, although control subjects could differentiate between entered and unentered arms without difficulty, animals with lesions were unable to exhibit this distinction. Much of their memory for arms previously entered in a sequence was at chance level, regardless of the placement of the tested arm in the sequence. Some tendency toward increased errors with longer sequences of arm entries was noted. This may indicate that animals with lesions were susceptible to proactive interference from previous choices. Regardless, even without the opportunity to develop or exhibit response biases, animals lesioned in the mediodorsal nucleus were unable to perform this win-shift task reliably. Thus, discrimination among maze arms is impaired after lesion of the mediodorsal nucleus and this impairment is independent of the motor response patterns which emerge during solution of a conventional radial maze task.