James B. Ranck

Electrophysiological characteristics of hippocampal complex-spike cells and theta cells

SummaryStimulating electrodes were chronically implanted in the ventral hippocampal commissure and the entorhinal cortex or angular bundle of rats. Moveable metal microelectrodes which could be passed through the hippocampus were implanted. All hippocampal units were classified as complex-spike cells or theta cells on the basis of the form of their action potentials and their rates of firing in various behaviors. Field potentials and unit firing evoked from the stimulating electrodes were recorded during slow wave sleep.Complex-spike cells (1) could often be antidromcally activated in CA3 (it was not attempted in CA1); (2) could only be induced to fire one or two action potentials in response to a single stimulus; (3) had action potentials at the same time as the local population-spike and, in condition-test studies, were depressed when the population-spike was depressed. (The population-spike is presumably the summed synchronous action potentials of pyramidal cells.)Theta cells: (1) were antidromically activated in only one out of 25 cases; (2) usually could fire long bursts of action potentials in response to a sufficiently intense single stimulus; (3) this firing occurred before, during, and after the local orthodromic population-spike.Most complex-spike cells in Ammons horn must be pyramidal cells (projection cells), and vice versa. The case for theta cells is more difficult. Some are non-pyramidal cells with locally ramifying axons, but at least some are projection cells. The data is consistent with most of them being inhibitory interneurons, but this is not established.

Localization and anatomical identification of theta and complex spike cells in dorsal hippocampal formation of rats

Abstract Microelectrodes were passed through the dorsal hippocampal formation of unrestrained rats, recording for at least 5 min each 35.3 μm. At each site the amplitude and duration of action potential spikes, frequency of firing, relation to slow wave theta rhythm, and presence of complex spikes or theta cells was recorded. One thousand and fourteen neurons were recorded from. (When recording from many neurons simultaneously, the “number” of the neurons was “counted” in an arbitrary and approximate way.) Of 949 nontheta cells greater than 80 μV amplitude, only one was not in the hilus of fascia dentata or in a layer of cells which overlapped stratum pyramidale and stratum granulosum. These are the locations of the cell bodies of projection cells (pyramidal cells and granule cells). However, this layer is, up to 400 μm thicker than stratum pyramidale. Theta cells were seen in sites of cell bodies of projection cells and also in stratum oriens of CA1, suprapyramidal layers of CA3, and dorsal part of the hilus of fascia dentata. The frequency of occurrence in these locations corresponded to the distribution of cell bodies of interneurons. We conclude that the class of projection cells and the class of nontheta cells have a very large overlap, and that the class of interneurons and the class of theta cells have a very large overlap.

Hippocampal theta rhythm and the firing of neurons in walking and urethane anesthetized rats

SummaryRecordings were taken from single neurons in the hippocampus and dentate gyrus of rats during walking and urethane anesthesia. Firing histograms for these cells were constructed as a function of the phase of the concurrent extracellularly recorded hippocampal slow wave theta rhythm. Care was taken to be sure of the site of recording of the theta rhythm and its phase with respect to a reliable reference, so that comparisons of the phases of firing could be made across animals. The firing of most of these neurons is deeply modulated as a function of the phase of the theta rhythm. This is true whether the theta rhythm occurs during walking or during urethane anesthesia, but for some types of cells the mean phases of firing are different in the two types of theta rhythm. During walking, pyramidal cells and interneurons in all hippocampal subregions and dentate granule cells have a maximum probability of firing near the positive peak of the theta rhythm recorded in the outer molecular layer of the dentate (dentate theta). During urethane anesthesia, the maximum firing probability for interneurons in CA1 and for dentate granule cells occurs near the negative peak of the dentate theta, while the phases of maximum firing for pyramidal cells and interneurons in CA3 and CA4 become widely distributed. The phases of maximum firing of pyramidal cells in CA1 are, if anything, more narrowly distributed around the positive peak of the dentate theta during urethane anesthesia than during walking. These differences in the firing of hippocampal cells during walking and urethane anesthesia represent some of the differences in cellular mechanisms distinguishing two kinds of hippocampal theta rhythm.

Head direction cells: properties and functional significance

The strong signal carried by head direction cells in the postsubiculum complements the positional signal carried by hippocampal place cells; together, the directional and positional signals provide the information necessary to permit rats to generate and carry out intelligent, efficient solutions to spatial problems. Our opinion is that the hippocampal positional system acts as a cognitive map and that the role of the directional system is to put the map into register with the environment. In this way, paths found using the map can be properly executed. Head direction cells have recently been discovered in parts of the thalamus reciprocally connected with the postsubiculum; such cells provide important clues to the organization of the directional system.

Hippocampal excitability phase-locked to the theta rhythm in walking rats

Abstract Measures of monosynaptic activation of the CA1 and dentate regions of the hippocampus varied with the phase of the slow-wave theta rhythm in freely moving rats. Despite the fact that the theta rhythm recorded in CA1 is phase-reversed with respect to that recorded in the dentate region, peak excitability in both regions occurred about 110° after the positive peak of the dentate theta rhythm.

Prevention of supersensitivity in partially isolated cerebral cortex

Abstract 1. 1. A portion of the marginal gyrus of the cerebral cortex on each of fifteen cats was undercut 3–4 mm deep. In terminal experiments under chloralose, 2–18 weeks later, local electrical stimulation produced after-discharges (in 12 cats) which had a longer duration on the undercut side than on the intact side. 2. 2. Another group of seventeen cats, each with an undercut marginal gyrus, received daily electrical stimulation (subthreshold for after-discharges) of the undercut cortex starting 1 week after undercutting (6 weeks delay in two cats). Total stimulation was about 400 applications at 0.6 mA, 400 at 0.8 mA and 200 at 1.0. mA. In terminal experiments under chloralose 1 week after the end of stimulation (6 weeks for one cat), fourteen of these cats did not show supersensitivity of the undercut cortex. 3. 3. These results suggest that chronic electrical stimulation can prevent the development of supersensitivity.

Macroelectrode Responses with Stimulation and Recording within Hippocampus and Related Structures during Different States of Consciousness

Abstract Three or four pairs of bipolar electrodes were chronically implanted in the hippocampal formation, subicular area, and entorhinal cortex of rats, all on the same side. The EEG, EOG, and neck EMG were also recorded. Responses due to electrical stimulation of one electrode pair were recorded in the other electrode pairs during slow-wave sleep, paradoxical sleep, and arousal. The stimuli were single, constant current pulses once every 5 sec. Most responses did not change with different states of consciousness. All responses which were smaller during paradoxical sleep than during slow-wave sleep were also small during arousal. Most changes were in this category. All of the responses which were larger during paradoxical sleep than in slow-wave sleep were the same in arousal and slow-wave sleep. Responses in hippocampus or fascia dentata from stimulation of other parts of these structures often changed, usually decreasing during paradoxical sleep and arousal. Responses in subiculum, presubiculum, or entorhinal cortex from stimulation of hippocampus or fascia dentata usually changed, usually decreasing with paradoxical sleep and arousal. Responses in entorhinal cortex or presubiculum from stimulation of subiculum increased in paradoxical sleep. Responses in fornix and CA3 from stimulation of presubiculum decreased in paradoxical sleep. An important negative finding was that no responses due to stimulation of entorhinal cortex changed in different states of consciousness. No clear correlation of the changes with phasic phenomena of paradoxical sleep was seen.

Measurement of the Topological Dimension of Hippocampal Place Cell Activity

The fundamental property of topological dimension of neural activity has never been measured before. We measured the topological dimension of the activity of 89 rat hippocampal place cells recorded during foraging using the neighborhood boundary countdown method. Points were rate vectors forming a manifold in an 89 dimensional rate space Since a boundary has one less dimension than the neighborhood it encloses, reducing the dimension in sequential radial cuts finally arrives at boundary that is two points. The number of cuts required is the topological dimension of the set. Due to sparsity, we used a shell-like boundary with thickness. As expected, we found the large inductive dimension of this set of points to be two. To examine the robustness of the method, we used both real and modeled place cells and varied the number of neurons, duration of the time step and smoothing, radius and thickness for the boundary, decrement of the radius with each cut, requirements for the center point, and number of points in the final cluster. With the exception of shell thickness, the result was insensitive to these variations. Knowing the topological dimension allows application of rigorous topological principles to the activity of neuron populations. The method potentially can be applied to other neural classes and other behaviors, to enumerate firing variables when they are unknown, even count the factors influencing neural activity in sleep.