Denis Boire

Relative Size of the Hyperstriatum ventrale Is the Best Predictor of Feeding Innovation Rate in Birds

Within the avian telencephalon, the dorsal ventricular ridge (DVR) contains higher order and multimodal integration areas. Using multiple regressions on 17 avian taxa, we show that an operational estimate of behavioral flexibility, the frequency of feeding innovation reports in ornithology journals, is most closely predicted by relative size of one of these DVR areas, the hyperstriatum ventrale. Neither phylogeny, juvenile development mode, nor species sampled account for the relationship. Similar results are found when the hyperstriatum ventrale is lumped with a second DVR structure, the neostriatum. In simple correlations, size of the wulst and the striatopallidal complex is associated with feeding innovation rate, but the two structures are eliminated from the multiple regressions. Our results parallel those on primates showing a correlation between innovation rate and neocortex size and support the idea that the mammalian neocortex and the neostriatum-hyperstriatum ventrale complex in birds have similar integrative roles.

Audition differently activates the visual system in neonatally enucleated mice compared with anophthalmic mutants.

The occipital cortex, normally visual, can be activated by auditory or somatosensory tasks in the blind. This cross‐modal compensation appears after early or late onset of blindness with differences in activation between early and late blind. This could support the hypothesis of a reorganization of sensory pathways in the early blind that does not occur in later onset blindness. Using immunohistochemistry of the c‐Fos protein following a white noise stimulus and injections of the anterograde tracer dextran‐biotin in the inferior colliculus, we studied how the occurrence of blindness influences cross‐modal compensation in the mutant anophthalmic mouse strain and in C57BL/6 mice enucleated at birth. We observed, in mutant mice, immunolabeled nuclei in the visual thalamus – the dorsal lateral geniculate nucleus – in the primary visual area (V1) and a few labeled nuclei in the secondary visual area (V2). In enucleated mice, we observed auditory activity mainly in V2 but also sparsely in V1. No labeled cells could be found in the visual thalamus. Tracing studies confirmed the difference between anophthalmic and birth‐enucleated mice: whereas the first group showed inferior colliculus projections entering both the dorsal lateral geniculate and the latero‐posterior nuclei, in the second, auditory fibers were found only within the latero‐posterior thalamic nucleus. None was found in controls with intact eyes. We suggest that the prenatal period of spontaneous retinal activity shapes the differences of the sensory reorganization in mice.

Chapter 28 When the auditory cortex turns visual

Abstract We studied visually guided behavior and the visual response properties of single auditory cortex (A1) neurons in neonatally operated hamsters with surgically induced, permanent, ectopic retinal projections to auditory thalamic nuclei and to visual thalamic nuclei which normally receive little direct retinal input. The surgically induced retino-thalamo-cortical pathways can mediate visual guided behaviors whose normal substrate, the pathway from the retina to the primary visual cortex via the primary thalamic visual nucleus, is missing. The visually evoked response properties of A1 neurons resemble in many respects those of neurons in V1 of normal hamsters: many A1 neurons have well-defined visual reseptive fields and preferences for orientation or direction of movement. In addition, some visually responsive cells in A1 are bimodal — they also respond to auditory stimuli. The visually responsive neurons in A1 probably account for the capacity of the auditory cortex to mediate visual behavior in ‘rewired hamsters’.

Quantitative Analysis of the Retinal Ganglion Cell Layer in the Ostrich, Struthio camelus

The total number, distribution and peak density of ganglion cells were evaluated in the Nissl-stained retina of the ostrich (Struthio camelus). The mean (n = 4) total number of retinal ganglion cells (RGC) was estimated at 2,274,128 (s.d. = 273, 152). The ostrich retina exhibited a prominent horizontal visual streak along which a central area located nasal to the pecten had a peak density of 9,500 cells/mm2. A high concentration of cells with a peak density of 2,646 cells/mm2 was also observed in the temporal retina, slightly dorsal to the visual streak. The results further showed that the ostrich eye has a 15-mm pupil entrance diameter, its mean axial length is 39.81 mm, the estimated retinal magnification factor is 0.4075 mm/deg and the maximum visual acuity along the well-defined visual streak was estimated to be 19.32 cycles/deg. The latter component of the retina might subserve vision along the horizon while the temporal region mediates binocular processing. The data also showed that the degree of retinal illumination in this bird could be comparable to that noted in some nocturnal species. The findings in this study suggest that the ostrich might not be restricted to diurnal activity.

Cortical and subcortical projections to primary visual cortex in anophthalmic, enucleated and sighted mice

The purpose of this study was to identify and compare the afferent projections to the primary visual cortex in intact and enucleated C57BL/6 mice and in ZRDCT/An anophthalmic mice. Early loss of sensory‐driven activity in blind subjects can lead to activations of the primary visual cortex by haptic or auditory stimuli. This intermodal activation following the onset of blindness is believed to arise through either unmasking of already present cortical connections, sprouting of novel cortical connections or enhancement of intermodal cortical connections. Studies in humans have similarly demonstrated heteromodal activation of visual cortex following relatively short periods of blindfolding. This suggests that the primary visual cortex in normal sighted subjects receives afferents, either from multisensory association cortices or from primary sensory cortices dedicated to other modalities. Here cortical afferents to the primary visual cortex were investigated to determine whether the visual cortex receives sensory input from other modalities, and whether differences exist in the quantity and/or the structure of projections found in sighted, enucleated and anophthalmic mice. This study demonstrates extensive direct connections between the primary visual cortex and auditory and somatosensory areas, as well as with motor and association cortices in all three animal groups. This suggests that information from different sensory modalities can be integrated at early cortical stages and that visual cortex activations following visual deprivations can partly be explained by already present intermodal corticocortical connections.

Indirect pathway between the primary auditory and visual cortices through layer V pyramidal neurons in V2L in mouse and the effects of bilateral enucleation

Visual cortical areas are activated by auditory stimuli in blind mice. Direct heteromodal cortical connections have been shown between the primary auditory cortex (A1) and primary visual cortex (V1), and between A1 and secondary visual cortex (V2). Auditory afferents to V2 terminate in close proximity to neurons that project to V1, and potentially constitute an effective indirect pathway between A1 and V1. In this study, we injected a retrograde adenoviral vector that expresses enhanced green fluorescent protein under a synapsin promotor in V1 and biotinylated dextran amine as an anterograde tracer in A1 to determine: (i) whether A1 axon terminals establish synaptic contacts onto the lateral part of V2 (V2L) neurons that project to V1; and (ii) if this indirect cortical pathway is altered by a neonatal enucleation in mice. Complete dendritic arbors of layer V pyramidal neurons were reconstructed in 3D, and putative contacts between pre‐synaptic auditory inputs and postsynaptic visual neurons were analysed using a laser‐scanning confocal microscope. Putative synaptic contacts were classified as high‐confidence and low‐confidence contacts, and charted onto dendritic trees. As all reconstructed layer V pyramidal neurons received auditory inputs by these criteria, we conclude that V2L acts as an important relay between A1 and V1. Auditory inputs are preferentially located onto lower branch order dendrites in enucleated mice. Also, V2L neurons are subject to morphological reorganizations in both apical and basal dendrites after the loss of vision. The A1–V2L–V1 pathway could be involved in multisensory processing and contribute to the auditory activation of the occipital cortex in the blind rodent.

Subcortical auditory input to the primary visual cortex in anophthalmic mice

Anatomical and imaging studies show ample evidence for auditory activation of the visual cortex following early onset of blindness in both humans and animal models. Anatomical studies in animal models of early blindness clearly show intermodal pathways through which auditory information can reach the primary visual cortex. There is clear evidence for intermodal corticocortical pathways linking auditory and visual cortex and also novel connections between the inferior colliculus and the visual thalamus. A recent publication [L.K. Laemle, N.L. Strominger, D.O. Carpenter, Cross-modal innervation of primary visual cortex by auditory fibers in congenitally anophthalmic mice, Neurosci. Lett. 396 (2006) 108-112] suggested the presence of a direct reciprocal connection between the inferior colliculus and the primary visual cortex (V1) in congenitally anophthalmic ZRDCT/An mice. This implies that this mutant mouse would be the only known vertebrate having a direct tectal connection with a primary sensory cortex. The presence of this peculiar pathway was reinvestigated in the ZRDCT/An mouse with highly sensitive neuronal tracers. We found the connections normally described in the ZRDCT/An mouse between: (i) the inferior colliculus and the dorsal lateral geniculate nucleus, (ii) V1 and the superior colliculus, (iii) the lateral posterior nucleus and V1 and between (iv) the inferior colliculus and the medial geniculate nucleus. We also show unambiguously that the auditory subcortical structures do not connect the primary visual cortex in the anophthalmic mouse. In particular, we find no evidence of a direct projection from the auditory mesencephalon to the cortex in this animal model of blindness.

Regional analysis of neurofilament protein immunoreactivity in the hamster's cortex.

The laminar distribution of several distinct populations of neurofilament protein containing neurons has been used as a criterion for the delineation of cortical areas in hamsters. SMI-32 is a monoclonal antibody that recognizes a non-phosphorylated epitope on the medium- and high-molecular weight subunits of neurofilament proteins. As in carnivores and primates, SMI-32 immunoreactivity in the hamster neocortex was present in cell bodies, proximal dendrites and axons of some medium and large pyramidal neurons located in cortical layers III, V and VI. A small population of labeled multipolar cells was also found in layer IV. Neurofilament protein immunoreactive neurons were found throughout isocortical areas. Very few labeled cells were encountered in supplemental motor area, insular cortex, medial portion of associative visual cortex and in parietal association cortex. Our data indicate that SMI-32 immunoreactive cells can be efficiently used to trace boundaries between neocortical areas in the hamsters brain. The regional distribution SMI-32 immunoreactivity in the hamster cortex corresponds quite closely with cortical areas as defined by their cytoarchitecture and myeloarchitecture. The primary sensory cortical areas contain the most intense of SMI-32 immunoreactivity and are also those with the highest density of myelinated axons. Very low SMI-32 immunoreactivity was found in orbital, insular, perirhinal, cingulate and infralimbic cortices, which are also poor in myelinated axons. This supports the association between SMI-32 immunoreactivity and myelin contents.

Retinal projections in the cat: A cholera toxin B subunit study

The B fragment of cholera toxin (CTb) is a highly sensitive anterograde tracer for the labelling of retinal axons. It can reveal dense retinofugal projections to well-known retinorecipient nuclei along with sparse but distinct input to target areas that are not commonly recognized. Following a unilateral injection of CTb into the vitreous chamber of seven adult cats, we localized the toxin immunohistochemically in order to identify direct retinal projections in these animals. Consistent with previous findings, the strongest projections were observed in the superficial layers of the superior colliculus, the dorsal and ventral lateral geniculate nuclei, the pretectal nuclei, the accessory optic nuclei, and the suprachiasmatic nucleus of the hypothalamus. However, we also found labelled terminals in several other brain areas, including the zona incerta, the medial geniculate nucleus, the lateral posterior-pulvinar complex, the lateral habenular nucleus, and the anterior and lateral hypothalamic regions. The morphological characteristics of the retinal axon terminals in most of the identified novel target sites are described.

Transneuronal degeneration of retinal ganglion cells in early hemispherectomized monkeys.

Transneuronal retrograde cell changes in the retina of the primate have been well documented after lesions to striate cortex, but little is known about the effects of hemispherectomy, a surgical procedure used in humans for the treatment of intractable epilepsy. In order to follow the time course of this degenerative process, we examined the retinae of six monkeys who underwent a total hemispherectomy at various postnatal ages with a survival period of 4 years. We demonstrate that transneuronal retrograde degeneration in the retina following hemispherectomy is inversely correlated with age at the time of the lesion. This degeneration is maximal when the lesion is induced within the first 4-6 months of life and less pronounced from 8 months to adulthood.