James L. Ringo

Neuronal Interconnection as a Function of Brain Size

The effect of increasing brain size upon the degree of interconnection between neurons is analyzed. An explicit model suggests that as the brain is scaled up there must be a corresponding fall in percent connectedness (the fraction of cells with which any one cell communicates directly). The reason for this is that if the percent connectedness is to be maintained in the face of increased neuron number, than a large fraction of any brain size increase would be spent maintaining such interconnection while the increasing axon lengths would reduce neural computational speed. One implication is that larger brains, being necessarily limited in allowable interconnectedness, may tend to show more specialization.

Investigation of long term recognition and association memory in unit responses from inferotemporal cortex

We investigated recognition and association memory in the responses of single units isolated in the inferior temporal cortex of a macaque while it performed a visual discrimination task. The unit responses showed significant recognition memory (a decreased response upon image repetition). Furthermore, a recognition memory appeared to be a permanent feature in these units. Such memory was evident in responses recorded at least 1 h after the most recent presentations of the more familiar images and may have been built up over the months of training. For these cells, the shorter-term recognition memory (seconds) and the longer-term recognition memory (hour plus) were significantly correlated (0.68). In these same cells associative memory was investigated with ten abstract images which had been randomly and permanently paired. The monkey had been taught to discriminate these five pairs from other similar pairs of images. Neither the spike count nor temporal response shape (as determined by a principal-components analysis) showed increased similarity for the images that had been paired. The cells that had both short-term and long-term recognition memory had responses to previously paired stimuli that were no more similar than expected by chance.

Memory decays at the same rate in macaques with and without brain lesions when expressed in d′ or arcsine terms

Data from the literature on the effect of lesions upon recognition memory in the monkey have been examined. On the basis of percentage scores the published data can be interpreted as showing that the ability to recognize a previously seen object decays faster in macaques with brain lesions than it does in normal animals. A reanalysis of the extensive data in terms of d of Signal Detection Theory or by arcsine transform suggests, on the contrary, that the rate of decay from 0 to 600 s, is essentially the same in normal animals and in those with lesions (particularly temporal lobe lesions). Indeed, in d or arcsine terms, the effect of the lesions is fully developed at the shortest times used, and shows no increase as a function of the delay between initial presentation and test. Thus, very different conclusions stem from the choice of scale.

Stimulus specific adaptation in excited but not in inhibited cells in inferotemporal cortex of Macaque

Many cells in inferotemporal cortex respond more actively to a novel presentation than to a subsequent re-presentation of the same image, exhibiting stimulus specific adaptation (SSA). Previously, analysis of this adaptation was limited to visually excited cells, excluding visually inhibited cells. In the present experiment we studied 654 cells in four macaques performing visual tasks. Strong SSA (P < 0.0001) was observed in those cells which were excited by visual stimuli. This adaptation was also seen in the subset of such cells which, though excited by visual stimuli, failed to show visual specificity in their responses. Interestingly, no SSA (P > 0.1) was observed in the group of cells inhibited by visual stimuli. Furthermore, most inhibited cells failed to show visual specificity. This lack of visual specificity and SSA suggests that the visually inhibited cells have a limited role in the detailed information processing of visual perception and memory activated by the tasks used in the present experiments.

Seemingly discrepant data from hippocampectomized macaques are reconciled by detectability analysis.

Wide differences in the effects of hippocampectomy on the visual memory performances of monkeys have been reported in the literature. These differences have been attributed to the extent of preoperative training. Previous calculations, however, have always utilized data expressed as a percentage correct. A reanalysis based on detectability, the d of signal detection theory, suggests that the differences may be illusory. The losses in visual memory performance due to hippocampal lesions as measured in different laboratories are about equal in terms of d. This points out a potential trap in making direct comparison of absolute differences in percentage values.

A macaque remembers pictures briefly viewed six months earlier

While there are several studies documenting the enduring nature of memory for acquired discriminatory habits or skills in animals, comparable data on memory for visual scenes, i.e., events, are essentially non-existent, and difficult to obtain even in man. An opportunity to assay this question in macaques arose in the early stages of training an animal on a running recognition task. It had previously been trained on trial-unique delayed matching to sample, and its past experience with this visual material was precisely known. When some of these images which had not been seen by the monkey for at least 6 months were intermingled with comparable material during its training on the running recognition task, with a high degree of statistical reliability (P less than 0.005) it distinguished about one-third of the earlier images, many of which had been seen for a total of only 30 s or less. A medical student, who had previously trained the animals and had had more exposure to the material than did this macaque, and certainly had more precise instruction on how to perform, recognized two-thirds of these same images, also after a hiatus of 6 months. It thus appears likely that the permanence of mnemonic storage for briefly encountered scenes is comparable for the central visual systems of macaque and man.

Eye position-sensitive units in hippocampal formation and in inferotemporal cortex of the Macaque monkey

The activity of 330 hippocampal and inferotemporal cells was recorded while seated monkeys with fixed heads worked in a visual discrimination task. Monkeys had to move their eyes to one of five different positions to maintain gaze on an image. The image was then extinguished and the monkeys maintained a fixed gaze on the target position in darkness to obtain a reward. The five positions of image presentation were on a horizontal line, consisting of a centre position and lateral positions which were 10 and 20 degrees right and left of it.

Forebrain commissures and visual memory: a new approach.

The primary purpose of these exploratory experiments was to determine: (1) whether the forebrain commissures can provide full accessibility of the mnemonic store to either hemisphere when the taks involves memory for events (images) rather than, as in essentially all previous tests on split-brain animals, memory for rules (discrimination habits); and (2) whether the anterior commissure (AC) alone is capable of such function. Macaques, with optic chiasm transected to allow limitation of direct visual input to one or the other hemisphere, were trained on tasks requiring recognition of previously viewed photographic slides. For one task, delayed-matching-to-sample (DMTS), the animal was presented with a sample image, and then 0-15s later was required to choose that image in preference to a second image concurrently displayed. On the other task, running recognition (RR), a series of images was presented, some of which were repetitions of images previously seen in that session, and the animal was required to signal its recognition of these repetitions. For either task the initial presentation could be made to one eye and hemisphere, and subsequent recognition required of the other. In such circumstance, if all forebrain commissures were divided, such interhemispheric recognition was no longer possible. For the DMTS task if either the AC or 5 mm of the splenium of the corpus callosum were available, interhemispheric recognition was basically equivalent to that using the same eye and hemisphere. However, interhemispheric accuracy with the RR task, while well above chance levels, was consistently inferior to that achieved intrahemispherically when complex scenes or objects were viewed. This is probably a consequence mostly of the differing visual fields of the two eyes, since interhemispheric accuracy was greatly improved by use of images having approximately identical right and left halves. No consistent hemispheric specialization nor difference in direction of interhemispheric communication was observed despite the use of different types of material and the different mnemonic tasks. It is concluded that the AC in macaques can achieve full and continuously operative neural unification of the mnemonic traces of past experience.

Saccadic eye movements, even in darkness, generate event-related potentials recorded in medial septum and medial temporal cortex

Saccadic eye movements (saccades) in primates organize the visual information about the environment into a pulsatile course. Recent studies from our laboratory have found substantial single unit activity, of extra-retinal origin, in medial temporal and inferotemporal cortex with each saccade (even in the dark). In the current experiment we studied event-related potentials to spontaneous saccades from electrodes in medial temporal cortex as well as medial septum. Significant event-related potentials were recorded in both regions (again even in the dark). These data suggest that higher-level processing itself may synchronize with saccades.

Interhemispheric sharing of visual memory in macaques.

(1) In macaques with the optic chiasm transected, and forebrain commissural communication limited to the anterior commissure or the posterior 5 mm of the splenium of the corpus callosum, visual patterns viewed initially by only one eye (hemisphere) are subsequently recognized by the other with normal accuracy. (2) The efficiency of these commissural paths is further indicated by the fact that even when as many as six target images are presented for memorization to only one hemisphere, it makes essentially no difference as to accuracy or latency of performance which hemisphere is then required to distinguish target from non-target images. (3) By electrically tetanizing structures in one or the other temporal lobe at various times in relation to visual input and/or mnemonic testing it could be shown: (a) that a memory trace restricted in its formation to a single hemisphere was available to the other via either forebrain commissure, and (b) that the memory is formed bilaterally despite unilateral input. (4) When the chiasm is split but the commissures are intact, simultaneous presentation of disparate images to each hemisphere severely perturbs performance, suggesting that the callosal system operates continuously to unify visual percepts; but when only the anterior commissure is intact, the two hemispheres accept incongruent images without perturbation. (5) In the fully split-brain condition, when one hemisphere cannot access memories held in the other, the accuracy of performance by each hemisphere is nevertheless burdened by the memory load of its neocortically disconnected partner. It can thus be inferred that the brainstem plays a critical, unifying role in this mnemonic process.