Leo M. Chalupa

Responses of visual, somatosensory, and auditory neurones in the golden hamster's superior colliculus

1. The response characteristics of visual, somatosensory, and auditory neurones in the golden hamsters superior colliculus were investigated.

Differentiation of brain stem loci which affect hippocampal and neocortical electrical activity

Abstract Systematic mapping by high frequency stimulation (100 Hz) of the brain stem of cats maintained under a mixture of nitrous oxide and oxygen has revealed five somewhat delimited and dispersed sites where stimulation caused hippocampal theta rhythm (synchrony) and two where a contrasting pattern of desynchronization was elicited. The theta-producing sites were found in nucleus reticularis pontis oralis, nucleus locus coeruleus, the giant cell region of the pontine tegmental field, the midbrain tegmentum, and in the ventrolateral portion of the periaqueductal gray substance. The two desynchronizing sites were localized in nucleus reticularis pointis caudalis and in the nuclei of the raphe. The synchronizing sites differed with respect to the frequency of the theta rhythm induced in the hippocampus. Usually, when the hippocampus displayed a synchronized theta rhythm the electrical activity of the neocortex was desynchronized and vice versa, however, there were exceptions in which either the anterior or posterior neocortex displayed a thetalike rhythm while the hippocampus was in either a synchronized or desynchronized state. These findings have been discussed in terms of possible multiple systems of brain stem influence upon hippocampus and neocortex and it is suggested that such ascending systems may be responsible for differential states of activation and arousal.

Uniformity of cell distribution in the ganglion cell layer of prenatal cat retina: Implications for mechanisms of retinal development

Abstract In an attempt to understand the ontogeny of the topography of the ganglion cell layer of the adult cat, we have studied the distribution of ganglion cells and their presumed percursor cells in pre- and postnatal retinas. Cell distribution was studied in whole-mounted, cresyl violet-stained retinas of fetuses of embryonic ages E47 and E57, of new-born animals, and of the adult. At E47 many cells, presumably the precursors of ganglion cells and of other neurones of the inner layers of the retina, have migrated from the germinative ventricular layer of the retina to the future ganglion cell layer. However, neither of the major features of the topography of the adult retina, the area centralis and visual streak, is apparent. The precursor cells are very numerous (our estimate is 860,000 as against about 116,250 ganglion cells in the adult retina), and apparently uniformly distributed. Their appearance is quite immature, with little cytoplasm evident. By E57, many cells have acquired granular cytoplasm and the area centralis and visual streak are clearly recognisable. Indeed, an 18:1 gradient in ganglion cell density has developed between central and peripheral retina, although the retina has only doubled in area. At birth the topography of the ganglion cell layer has matured considerably, although the number of cells identified as ganglion cells is higher than in the adult. These results suggest that an important mechanism in the development of the area centralis is a process of ‘differential maturation’ in which there is a marked variation between the area centralis and peripheral retina in the proportion of precursor cells which survive and mature as ganglion cells. The high number of ganglion cells in the neonatal retina suggests that this process continues into early postnatal life. A process of differential growth of the retina, suggested by earlier workers, seems also to contribute to the adult pattern of retinal topography.

The laminar distribution of cortical connections with the tecto- and cortico-recipient zones in the cat's lateral posterior nucleus

The anterograde and retrograde transport of wheat germ agglutinin congugated to horseradish peroxidase was used to examine the laminar organization of cortical connections with the two visual zones that comprise the cats lateral posterior nucleus. Microelectrophoretic deposits of the tracer into the principal tecto-recipient zone in the medial division of the lateral posterior nucleus revealed reciprocal connections with the following cortical fields: areas 19 and 21a, the medial and lateral banks of the middle suprasylvian sulcus, and the dorsal and ventral banks of the lateral suprasylvian sulcus, which correspond to the dorsal lateral suprasylvian and ventral lateral suprasylvian visual areas of Palmer et al. [(1978) Brain Res. 177, 237-256] and an area in the fundus of the posterior suprasylvian sulcus. In each of these cortical areas two distinct populations of cells were labeled, small pyramidal neurons in layer VI and large pyramidal cells in layer V. Overlying these backfilled cells were two bands of anterograde label, a narrow strip in layer I and a wide band centered in layer IV. Deposits of wheat germ agglutinin conjugated to horseradish peroxidase confined to the striate-recipient zone in the lateral portion of the lateral posterior nucleus resulted in cortical label in areas 17, 18, 19, 20a and b, 21a, the medial and lateral banks of the middle suprasylvian sulcus, the posterior suprasylvian sulcus and in the fundus of the splenial sulcus. In all cortical areas other than 17 and 18, the laminar distribution of label was the same as that found after deposits of the tracer into the medial division of the lateral posterior nucleus. In contrast, areas 17 and 18 contained backfilled cells that were confined to layer V and anterograde label that was restricted to layer I. These findings indicate that the cortical areas that receive a direct projection from the A laminae of the dorsal lateral geniculate nucleus maintain a distinct laminar organization of reciprocal connections with the extrageniculate visual thalamus. Conversely, all other visual areas of the cortex share a common pattern of reciprocal connections with both the tecto- and striate-recipient zones of the lateral posterior nucleus.

A review of cat and monkey studies implicating the pulvinar in visual function.

The anatomical, neurophysiological, and behavioral evidence implicating the cats and monkeys pulvinar in visual function is reviewed. While at present it is not possible to establish homologies between regions of the posterior thalamus in these two species, in both species there is evidence for extra-geniculate pathways by which visual input could be relayed to cortex. In the monkey, it is suggested that the inferior pulvinar could be part of a subcortical system dealing with visual attentional function, while portions of the medial pulvinar could be involved in a system concerned with oculomotor integration.

Temporal sequence of neurotransmitter expression by developing neurons of fetal monkey visual cortex

The developing fetal monkey visual cortex was studied immunocytochemically from 110-155 days post-conception in order to localize cell populations immunoreactive (ir) for gamma-aminobutyric acid, Substance P, cholecystokinin-octapeptide, somatostatin, neuropeptide Y, and proenkephalin A peptide (BAM-18). The area 17/18 border and all cortical laminae identified in the adult visual cortex were discernible from the youngest age examined. All ir-cell populations studied were present at each fetal age. However, despite a relatively adult-like cytoarchitecture, all ir-cell populations studied displayed patterns of immunostaining which were unlike those described in adult visual cortex, and showed significant changes in laminar distribution, morphology, and numbers over the time course of gestation examined. Despite the differences in the patterns of immunostaining between the fetal and adult visual cortex, ir-cell populations intrinsic to the developing visual cortex exhibited adult-like combinations of co-localized transmitters and peptides. The developing monkey cortex also contains ir-cell populations, particularly BAM-18-ir cells, which have not been detected immunocytochemically in the adult monkey cortex. Differences between the fetal and the adult ir-cell populations might be accounted for by cell death, morphological transformation, secondary migration or changes in gene expression for neurotransmitters and neuropeptides.

Callosal projection neurons in area 17 of the fetal rhesus monkey

We have studied the distribution of callosal projection neurons in area 17 of a fetal rhesus monkey which received large injections of horseradish peroxidase into the contralateral occipital cortex. In comparison to other cortical areas, area 17 contains few callosal projection neurons. Most of these cells are confined to a region extending tangentially about 2.5 mm from the 17/18 border, although a few neurons were noted as much as 5 mm from the border. Comparing the distribution of callosal projection neurons in the fetal monkey with what has been described in newborn and adult macaques, it is apparent that although some degree of refinement in striate callosal connections may occur during in utero development, the prenatal development of callosal connections in the macaque is inherently adult-like.

High precision systems require high precision “blueprints”: A new view regarding the formation of connections in the mammalian visual system

It is well established that early in development interconnections within the mammalian visual system are often more widespread and less precise than at maturity. The literature dealing with the formation of visual connections has largely ignored differences in developmental specificity among species differing in their phylogenetic status and/or the visual ecological niche that they occupy. Based on a review of the available evidence, we have formulated an hypothesis to account for the varying degrees of developmental specificity that characterize different visual systems. It is suggested that extremely precise systems required for high-acuity binocular vision exhibit fewer presumed developmental errors than do visual systems characterized by poorer acuity and relatively crude depth perception. The developmental implications of the hypothesis are considered, and specific experiments are proposed to further test its validity.

Retinal waves in mice lacking the β2 subunit of the nicotinic acetylcholine receptor

The structural and functional properties of the visual system are disrupted in mutant animals lacking the β2 subunit of the nicotinic acetylcholine receptor. In particular, eye-specific retinogeniculate projections do not develop normally in these mutants. It is widely thought that the developing retinas of β2−/− mutants do not manifest correlated activity, leading to the notion that retinal waves play an instructional role in the formation of eye-specific retinogeniculate projections. By multielectrode array recordings, we show here that the β2−/− mutants have robust retinal waves during the formation of eye-specific projections. Unlike in WT animals, however, the mutant retinal waves are propagated by gap junctions rather than cholinergic circuitry. These results indicate that lack of retinal waves cannot account for the abnormalities that have been documented in the retinogeniculate pathway of the β2−/− mutants and suggest that other factors must contribute to the deficits in the visual system that have been noted in these animals.

Dendrites of rod bipolar cells sprout in normal aging retina

The aging nervous system is known to manifest a variety of degenerative and regressive events. Here we report the unexpected growth of dendrites in the retinas of normal old mice. The dendrites of many rod bipolar cells in aging mice were observed to extend well beyond their normal strata within the outer plexiform layer to innervate the outer nuclear layer where they appeared to form contacts with the spherules of rod photoreceptors. Such dendritic sprouting increased with age and was evident at all retinal eccentricities. These results provide evidence of retinal plasticity associated with normal aging.