Direct projection from the visual associative cortex to the caudate nucleus in the feline brain.

Recent morphological and physiological studies support the assumption that the extrageniculate ascending tectofugal pathways send visual projection to the caudate nucleus (CN) in amniotes. In the present study we investigate the anatomical connection between the visual associative cortex along the anterior ectosylvian sulcus (AES) and the CN in adult domestic cats. An anterograde tracer - fluoro-dextrane-amine - was injected into the AES cortex. The distribution of labeled axons was not uniform in the CN. The majority of labeled axons and terminal like puncta was found only in a limited area in the dorsal part of the CN between the coordinates anterior 12-15. Furthermore, a retrograde tracer - choleratoxin-B - was injected into the dorsal part of the CN between anterior 12 and 13. We detected a large number of labeled neurons in the fundus and the dorsal part of the AES between the coordinates anterior 12-14. Based upon our recent results we argue that there is a direct monosynaptic connection between the visual associative cortex along the AES and the CN. Beside the posterior thalamus, the AES cortex should also participate in the transmission of the tectal visual information to the CN. This pathway is likely to convey complex information containing both sensory and motor components toward the basal ganglia, which supports their integrative function in visuomotor actions such as motion and novelty detection and saccade generation.

Direct synaptic connections between superior colliculus afferents and thalamo-insular projection neurons in the feline suprageniculate nucleus: a double-labeling study with WGA-HRP and kainic acid.

The suprageniculate nucleus (Sg) of the feline thalamus, which subserves largely unimodal sensory and orientation behavior, receives input from the deep layers of the superior colliculus (SC), and projects to the suprasylvian cortical areas, such as the anterior ectosylvian visual area and the insular visual area (IVA), which contain visually responsive neurons. Through a double tract-tracing procedure involving the injection of wheat germ agglutinin conjugated with horseradish peroxidase (WGA-HRP) into the IVA and the injection of kainic acid into the SC, this study sought to determine the nature of the synaptic relationship between the SC afferents and the thalamo-cortical projection neurons. WGA-HRP injections labeled numerous neurons in the Sg, while kainic acid injections destroyed many tectothalamic terminals in the Sg. The distributions of the WGA-HRP-labeled neurons and the degenerated axon terminals overlapped in the dorsal part of the Sg. Electron microscopic observations demonstrated that the degenerated axon terminals made synaptic contacts with the dendrites of the WGA-HRP-labeled neurons in this overlapping region of the Sg. These results provide the first anatomical evidence that the Sg may play a role in the key relay of visual information from the SC to the IVA, within an identified extrageniculo-cortical pathway.

A possible monosynaptic pathway links the pedunculopontine tegmental nucleus to thalamostriatal neurons in the hooded rat.

The thalamic lateral posterior nucleus (LP) of the hooded rat is regarded as a relay nucleus for the transmission of information from visuomotor-related structures such as the superior colliculus, pedunculopontine tegmental nucleus (PPT) and substantia nigra, pars reticulata, to visual cortical areas as well as the striatum. The aim of the present study was to examine the relationships of the thalamo-striatal projection neurons with the LP afferent fibers derived from the PPT, using injections of the anterograde tracer biotinylated dextran amine (BDA) and the retrograde tracer cholera toxin-B (CTB) into the PPT and the striatum, respectively. Findings showed that the location of terminals derived from PPT and LP neurons projecting to the striatum overlapped considerably in the ventral portion of the LP. Ultrastructural observations within this overlapped LP region showed that BDA-labeled terminals make synaptic contacts with dendrites of CTB-labeled neurons. The present results thus provide morphological support for the contention that information from the PPT neurons is relayed to the striatum through by the LP.

Multisensory responses and receptive field properties of neurons in the substantia nigra and in the caudate nucleus.

The basal ganglia are widely regarded as structures involved in sensorimotor co-ordination, but little is known about the sensory background of their function. We publish here descriptions of the excitatory sensory responses and receptive field properties of the visual, auditory, somatosensory and multisensory caudate nucleus and substantia nigra pars reticulata neurons. Altogether 111 caudate nucleus and 124 substantia nigra sensory neurons were recorded in halothane-anaesthetized, immobilized, artificially ventilated cats. The sensory properties of the caudate and nigral neurons were found to be quite similar. A majority of the units were unimodal while a significant proportion of them were multisensory. The visual and the somatosensory modalities predominated for both nuclei. The sensory receptive fields were extremely large. The visual and auditory receptive fields covered the whole physically approachable sensory field and the somatosensory receptive fields covered the whole body surface of the animal. The receptive field properties of the multisensory caudate and nigral units were similar to those of the unimodal neurons. We observed no signs of retinotopical or somatotopical organization within the basal ganglia. The particular sensory receptive field properties, together with the significant number of multisensory neurons in the basal ganglia, suggest the existence of a multisensory pathway of presumably tectal origin involving the caudate nucleus and the substantia nigra that may serve for the sensory feedback of motor actions co-ordinated by the basal ganglia.

Remodeling of reciprocal synapses associated with persistence of long-term memory.

We investigated a model of long-term memory in which the female mouse establishes pheromonal memory of its partner at mating. We examined the reciprocal synapses of the accessory olfactory bulb and found that pheromonal memory was associated with morphological changes in excitatory synapses in the early phase of memory acquisition and by changes in inhibitory synapses in the late phases of memory persistence. After extinction of pheromonal memory, these morphological changes were no longer present. These findings suggest that the persistence of pheromonal memory is associated with continuous and dynamic changes in the morphological plasticity of reciprocal synapses in the accessory olfactory bulb.

Two types of neuron are found within the PPT, a small percentage of which project to both the LM-SG and SC.

The pedunculopontine tegmental nucleus (PPT) projects its cholinergic fibers to both the lateralis medialis-suprageniculate nucleus (LM-Sg) and the superior colliculus (SC). For the purpose of verification of whether a single neuron in the PPT projects to both the LM-Sg and the SC, we injected dextran tetramethylrhodamine (DR) into the LM-Sg and dextran fluorescein (DF) into the ipsilateral SC. The DR-positive neurons labeled retrogradely in the PPT are small (mean: 27.13+/-1.22 micro m) and distributed in the rostral two-thirds of this nucleus, whereas the DF-positive neurons are small (mean: 27.54+/-1.16 micro m) or medium-sized (mean: 40.18+/-1.43 micro m), and are located throughout the PPT. Thirty-five percent of all labeled neurons are double-labeled and small. The present study indicates that the PPT projection to the LM-Sg in part involves neurons bifurcating to the SC.

Postnatal development of cholinergic afferents from the pedunculopontine tegmental nucleus to the lateralis medialis-suprageniculate nucleus of the feline thalamus.

The lateralis medialis-suprageniculate nuclear complex (LM-Sg) has been shown to receive cholinergic fibers from the pedunculopontine tegmental nucleus (PPT). The majority of terminals of these cholinergic fibers make simple synaptic contact with dendritic profiles, whereas some make contacts with the dendrites of projection neurons and GABAergic interneurons forming a glomerular synaptic complex. In the present study, we investigate the postnatal development of glomerular synaptic complexes in the LM-Sg in association with terminals of the PPT-thalamic projection fibers. We examined the postnatal development of cholinergic innervation as well as GABAergic interneuron innervation in the LM-Sg using antibodies against ChAT and GABA, respectively. Although choline acetyltransferase (ChAT)-positive neurons already exist in the PPT at birth (P0), ChAT-positive fibers in the LM-Sg were observed only after P7. These ChAT-positive fibers gradually increased in number, and almost reached the adult level by postnatal day 28 (P28). GABA-positive interneurons were scattered throughout the LM-Sg at P0, increased in size gradually and reached adult size by P14. Immature glomerulus-like synaptic arrangements appeared at P14. Definite glomeruli, in which ChAT-positive terminals are present, were observed at P28. These results emphasize that interneurons in the LM-Sg grow by P14, and then make neural circuits with cholinergic innervation within the glomerulus by 3-4 weeks.

Visual receptive field properties of neurons in the caudate nucleus.

Visual single-unit activity was recorded in the caudate nucleus of halothane-anaesthetized, immobilized, artificially respirated cats. Visually sensitive neurons were found in the dorsolateral part of the caudate body. A majority of the units responded optimally to small spot-like stimuli moving with velocities between 30 and 120 degrees /s. The receptive field of these units is large: it covers a major part of both the contra- and ipsilateral visual hemifields. No signs of retinotopy were observed. Most of the neurons display directional selectivity and are narrowly tuned to the direction of the moving stimulus. These physiological properties are consistent with recent morphological results that reveal multiple connections of the caudate nucleus with the superior colliculus through tecto-extrageniculo-thalamic pathways in the mammalian brain.

Rapid induction of Arc is observed in the granule cell dendrites in the accessory olfactory bulb after mating.

The activity-regulated cytoskeleton-associated protein (Arc), encoded by the immediate early gene arc, is enriched in the brain and is hypothesized to play a role in the activity-dependent neuronal plasticity in the hippocampus. In the present study, the time course of Arc expression during the post-mating period was determined immunocytochemically, and the localization of Arc in the neurons in the accessory olfactory bulb (AOB) of female mice after mating was analyzed using immunocytochemical electron microscopy. Transient increases in the number of Arc-immunoreactive cells were observed in the glomerular, mitral/tufted cell and granule cell layers of the AOB after mating. In particular, the increase in the granule cell layer was remarkable, and larger than the increases in the other layers. In addition, electron microscopic observation revealed that Arc immunoreactivity was in the dendrites of the granule cells 1.5 h after mating. These results indicate that expression of Arc protein is induced rapidly and transiently in granule cell dendrites after mating. It is postulated that Arc protein has a role in the neuronal plasticity of the AOB after mating.

Anisotropic functional connections between the auditory cortex and area 18a in rat cerebral slices.

We developed a new method to visualize the myeloarchitecture in fresh slices, and investigated the properties of the functional neural connections around the boundary between the primary auditory cortex (area 41) and area 18a in rat cerebral slices. A fresh slice illuminated by near-vertical light was observed with a CCD camera. The translucent images of the slice showed contrast patterns very similar to myeloarchitecture. The boundary between these areas was identified by the well-developed layer IV/V in area 41 but not in area 18a. Antidromic/presynaptic components of the field potentials stimulated and recorded across the areal boundary showed symmetric distribution, while the postsynaptic field potentials in the direction from area 41 to 18a were more prominent than those in the opposite direction in layer II/III. In contrast, the dominant direction of propagation of postsynaptic potentials was from area 18a to 41 in layer V. In the presence of 1 microM bicuculline, an inhibitor of GABA(A) receptors, the polysynaptic activities propagating from area 18a into 41 via layer V were elicited by stimulation of area 18a. The propagation measured by Ca(2+) imaging or field potential recordings was potentiated after both areas 18a and 41 were alternately stimulated several times.

Mating behavior induces differential Arc expression in the main and accessory olfactory bulbs of adult rats.

The expression of activity-related cytoskeleton-associated protein, Arc, could be useful as a marker for neuronal activity. We investigated Arc-immunoreactivity in both the accessory olfactory bulb (AOB) and the main olfactory bulb (MOB) of adult male rats in response to mating or exposure to female pheromones. Mating behavior strongly enhanced the Arc-immunoreactivity in the granule cell layer of the AOB. However, the enhancement of Arc-immunoreactivity by mating behavior was not observed in the MOB. These results showed that Arc-immunoreactivity was enhanced when the AOB received both afferent and efferent information during mating behavior. Hence, the expression of Arc in the AOB directly associates the pheromonal information with mating behavior. The AOB will provide a useful model to investigate the function of Arc protein.

A comparative immunocytochemical study of development and regeneration of chemosensory neurons in the rat vomeronasal system.

Vomeronasal neurons undergo continuous neurogenesis during development and after neuronal injury. We used immunocytochemical methods to compare different stages of the vomeronasal organ development to those of regeneration following vomeronasal nerve transection. At E15 and at 6 to 10 days after injury, nestin-positive cells were observed throughout the sensory epithelium. We did not find nestin immunoreactivity to be localized to the boundary region of the epithelium. The early appearance and wide distribution of nestin-positive cells suggests that they represent chemosensory precursor cells that develop and migrate vertically in the epithelium. Vomeronasal receptor cells degenerated 6 to 8 days after nerve transection, but axon terminals in the accessory olfactory bulb (AOB) continued to show the presence of the chemosensory specific marker (OMP) for up to ten days, a significant finding observed in this study. It is likely that the distance from the site of nerve transection may contribute to differences in the time course of anterograde and retrograde axon degradation. OMP-positive neurons were observed in the normal adult epithelium and to a much lesser extent 10-60 days after recovery from nerve transection. Axons from regenerated receptor cells did not reach the AOB during this time period. This failure to reestablish connections with target cells in the AOB could explain why OMP-positive cells were rarely observed among the regenerated cells in the vomeronasal epithelium.

Expression and regulation of the immediate-early gene product Arc in the accessory olfactory bulb after mating in male rat.

Recent studies of the accessory olfactory bulb have shown that the expression of immediate-early genes, e.g., c-fos, c-jun and egr-1, can be used as a marker of neuronal activity in response to pheromonal cues. In this study, we analyzed the expression pattern, in response to mating, of the novel immediate-early gene product Arc (an activity-regulated cytoskeleton-associated protein). Arc is hypothesized to play a role in activity-dependent neuronal plasticity in the hippocampus. In a control group of male rats, only a small number of Arc-immunoreactive cells were observed in the accessory olfactory bulb. In a mating group, however, a marked increase in the number of Arc-immunoreactive cells was observed only in the granule cell layer of the accessory olfactory bulb. The increase in the number of Arc-immunoreactive cells after mating was similar to that observed for other immediate-early genes. However, for the mating group, the increase in Arc-positive cells was limited to the granule cell layer. Granule cells have been shown to exhibit a strong synaptic plasticity in response to pheromonal stimulation. From these findings we suggest that Arc plays an important role in neuronal plasticity in the accessory olfactory bulb.