Synaptic distribution of afferents from reticular nucleus in ventroposterior nucleus of cat thalamus

This study was aimed at determining the synaptic circuitry that contributes to the alterations in thalamic function that accompany changes in behavioral states. The somatosensory sector of the thalamic reticular nucleus (RTN) was identified by microelectrode recording in cats and injected with Phaseolus vulgaris-leucoagglutinin (PHA-L). The axons of labeled RTN cells gave rise to collaterals within the RTN and continued into the dorsal thalamus where they terminated predominately in the ventral posterior lateral nucleus (VPL). After small injections in the upper limb representation of RTN, most labeled terminations in VPL were confined to its medial part, suggesting the presence of a topographic organization in the projection. Terminations were concentrated in localized, focal aggregations of boutons. Combined electron microscopic immunocytochemistry, using immunogold labeling for γ-aminobutyric acid (GABA), showed that the PHA-L labeled boutons were GABA-positive terminals that ended in symmetrical synapses. Eighty-two percent of these synapses were on dendrites of relay neurons, 8.5% on dendrites of interneurons, and 9.3% on somata. The terminals of RTN axons form the majority of axon terminals ending in symmetrical synapses in VPL. Their concentration on relay neurons probably underlies the capacity of the RTN projection to reduce background activity of VPL relay neurons in the awake state and to maintain oscillatory behavior of these neurons in drowsiness and early phases of Sleep. © 1995 Wiley-Liss, Inc.     

Projection of brain stem neurons to the perigeniculate nucleus and the lateral geniculate nucleus in the cat

Small horseradish peroxidase injections in the perigeniculate nucleus (PGN) or the lateral geniculate nucleus (LGN) gave retrograde labeling of many cells in the pontomesencephalic reticular formation (RF), the nuclei raphe dorsalis and centralis linearis, locus coeruleus, nucleus of the optic tract and nucleus parabigeminalis. Antidromic stimulation was used to identify neurons in the RF projecting to the PGN-LGN complex. Threshold mapping through the PGN and the LGN shows separate projection from the reticular formation to the PGN and the LGN.     

The fine structure of the perigeniculate nucleus in the cat

The fine structure of the cat's perigeniculate nucleus has been analyzed and compared to that of dorsal thalamic relay nuclei. Golgi preparations and electron micrographs of perigeniculate cells commonly show somatic spines. The most common presynaptic elements for these spines and for the adjacent perikaryal surfaces are relatively large axon terminals containing round synaptic vesicles and making multiple asymmetric contacts. These "RLD" terminals (so termed for their round vesicles, large average size of the terminals, and dark mitochondria) are also presynaptic to dendritic spines and shafts of proximal and secondary dendrites. Comparisons with adjacent parts of the dorsal lateral geniculate nucleus show that these RLD terminals are cytologically distinct from retinogeniculate terminals and that small numbers of RLD terminals also occur in the geniculate A laminae. Three other major classes of perigeniculate synaptic terminals, resemble major classes of terminals in the dorsal lateral geniculate nucleus. These include two types of terminal with flat or ovoid synaptic vesicles and dark mitochondria, "FD1" and "FD2" terminals, and a class of small terminal with densely clustered round vesicles and dark mitochondria, "RSD" terminals. RSD terminals, which resemble corticogeniculate axon terminals, represent the only class of perigeniculate terminal that does not contact perikarya. FD2 terminals resemble lateral geniculate presynaptic dendrites and participate in serial and triadic synaptic contacts, being both pre- and postsynaptic; however, in contrast to the arrangement characteristic of thalamic relay nuclei, these contacts do not occur within synaptic glomeruli. A fifth major class of perigeniculate presynaptic terminal has large flat or polymorphic synaptic vesicles and pale mitochondria. These "FP" terminals are seen infrequently in the lateral geniculate A laminae. Similarities between perigeniculate and lateral geniculate fine structure may relate in part to common sources of afferent input to the two nuclei.     

Synaptic targets of thalamic reticular nucleus terminals in the visual thalamus of the cat

A major inhibitory input to the dorsal thalamus arises from neurons in the thalamic reticular nucleus (TRN), which use gamma‐aminobutyric acid (GABA) as a neurotransmitter. We examined the synaptic targets of TRN terminals in the visual thalamus, including the A lamina of the dorsal lateral geniculate nucleus (LGN), the medial interlaminar nucleus (MIN), the lateral posterior nucleus (LP), and the pulvinar nucleus (PUL). To identify TRN terminals, we injected biocytin into the visual sector of the TRN to label terminals by anterograde transport. We then used postembedding immunocytochemical staining for GABA to distinguish TRN terminals as biocytin‐labeled GABA‐positive terminals and to distinguish the postsynaptic targets of TRN terminals as GABA‐negative thalamocortical cells or GABA‐positive interneurons. We found that, in all nuclei, the TRN provides GABAergic input primarily to thalamocortical relay cells (93–100%). Most of this input seems targeted to peripheral dendrites outside of glomeruli. The TRN does not appear to be a significant source of GABAergic input to interneurons in the visual thalamus. We also examined the synaptic targets of the overall population of GABAergic axon terminals (F1 profiles) within these same regions of the visual thalamus and found that the TRN contacts cannot account for all F1 profiles. In addition to F1 contacts on the dendrites of thalamocortical cells, which presumably include TRN terminals, another population of F1 profiles, most likely interneuron axons, provides input to GABAergic interneuron dendrites. Our results suggest that the TRN terminals are ideally situated to modulate thalamocortical transmission by controlling the response mode of thalamocortical cells. J. Comp. Neurol. 440:321–341, 2001. © 2001 Wiley‐Liss, Inc.     

The effect of midbrain reticular stimulation upon perigeniculate neurons activity during different states of the sleep-waking cycle in the cat

Electrical stimulation of the mesencephalic reticular formation in chronic cats induced state-dependent effects on spontaneous firing of perigeniculate neurons. Perigeniculate neurons fired at lower rates during slow wave sleep than during wakefulness of paradoxical sleep. The stimulation caused a firing decrease in slow wave sleep; an effect which faded during wakefulness and paradoxical sleep and was superseded by a firing increase during periods of eye movements in 30% of the neurons. The responsiveness of perigeniculate neurons to optic tract and visual cortex stimulation either remained unchanged or was enhanced during the reticular induced firing changes.     

Axon collaterals in the thalamic reticular nucleus from thalamocortical neurons of the rat ventrobasal thalamus

Thalamocortical relay neurons from the rat ventrobasal nucleus were identified physiologically and injected intracellularly with horseradish peroxidase. The axons of these cells were followed through serial sections in order to determine if collaterals were given off within the ventrobasal nucleus or the thalamic reticular nucleus. No local collaterals were seen in the ventrobasal nucleus, thus indicating that interactions between relay cells in this nucleus are minimal. Of axons that could be followed into the internal capsule, 76% gave off visible collaterals in the thalamic reticular nucleus. Half of these axons had collaterals showing extensive branching with the potential of innervating a large number of thalamic reticular neurons. The other half had short, simple branches of restricted extent. No correlations were found between the physiological properties of a cell and the existence or extent of axon collaterals. These results describe the anatomical basis for the initial part of a feedback loop through the thalamic reticular nucleus that provides the major inhibitory influence on rat ventrobasal neurons.     

Neuronal activity of cat thalamus reticular and relay nuclei

The interaction between the unit activity of the thalamic reticular and relay nuclei was investigated on cats immobilized with tubarine. It was shown that unit activity of the relay nuclei can be significantly modulated by stimulation of the n. reticul. By simultaneous recording (with two microelectrodes) of the activity of thalamic reticular neurons the relay unit activity can be suppressed; during peripheral and cortical stimulations the alternation of excitation-inhibition of the thalamic reticular and relay units can be observed; excitation of thalamic reticular units can be associated with excitation of the relay nuclei units. Such types of interaction may also exist during simultaneous recording (by two microelectrodes) of the activity of the relay units and putative interneurons. Sometimes IPSPs with short latency (1 ms) were evoked in the thalamic relay nuclei during thalamic reticular stimulation. The existence of direct monosynaptic inhibition of the relay unit activity by the thalamic reticular units as well as inhibition by the activation of the putative interneurons of the specific thalamic nuclei is suggested.     

Cardiac sympathetic afferent input onto neurons in nucleus ventralis posterolateralis in cat thalamus

Neurons receiving cardiac sympathetic afferent input were studied in the nucleus ventralis posterolateralis (VPL) of the cat thalamus. Animals were anesthetized with urethan-chloralose. Units in the VPL were classified into 3 classes; low-threshold mechanoreceptive (LTM), nociceptive specific (NS) and wide dynamic range (WDR) units. Units driven by electrical stimulation of the left inferior cardiac nerve (ICN) were not included in the population of LTM units, but 43.5% of NS units and 68.8% of WDR units were excited by this stimulation. Units exclusively responsive to cardiac sympathetic afferents were not found. Both NS and WDR units were located in the shell region of the caudal VPL. NS units responsive to cardiac sympathetic afferents had a circumscribed cutaneous receptive field in the area corresponding to tactile dermatomes C5-T13. WDR units receiving cardiac sympathetic afferent input had at least a part of their receptive fields in the same area. These results suggest that the shell region of the caudal VPL constitutes a thalamic link in a cardiac pain pathway, and that cardiac and cutaneous pain systems share a common projection locus in the VPL.     

Neuronal reactions of the reticular nucleus and adjacent thalamus structures in the cat to natural stimulation in a chronic experiment

Spike responses of 104 neurons of the nucleus reticularis thalami (R) and neighbouring thalamic nuclei to the acoustic stimuli, tactile and visual stimulation were studied in the chronic experiment. 29% of neurons responded to the acoustic stimulation and 11% of them were not specific to different acoustic stimuli. The minimal latency of the excitation to the acoustic stimulation was 12-37 ms and that of the inhibition--18-27 ms. The duration of the excitation in response to the acoustic stimulation was 50-250 ms and that of inhibition--27-190 ms. 16% of R neurons responded to the stimulation of different sensory systems. The majority of R neurons showed excitation in response to different stimuli and only 4-10% of neurons showed inhibition.     

The morphology of physiologically identified GABAergic neurons in the somatic sensory part of the thalamic reticular nucleus in the cat

Neurons with somatic sensory receptive fields were examined electrophysiologically in the thalamic reticular nucleus of the cat. All cells had receptive fields much larger than those of neurons in the ventral posterior nucleus and were driven by less readily defined somesthetic stimuli. Response latencies to peripheral or medial lemniscal stimulation were, on average, longer than in the ventral posterior nucleus and suggested activation of the reticular nucleus cells by collaterals of thalamocortical relay cell axons arising in the ventral posterior nucleus. When injected intracellularly with horseradish peroxidase, reticular nucleus cells displayed thin axons with intrareticular collaterals and diffuse branches through much of the ventral posterior and posterior thalamic nuclei. Dendrites ended in processes resembling synaptic terminals. Electron microscopic immunocytochemistry of the same part of the reticular nucleus revealed processes immunoreactive for glutamic acid decarboxylase and identifiable as both collateral axon terminals and presynaptic dendrites of GABAergic reticular nucleus cells. These synaptically linked reticular nucleus cells and, in addition, immunoreactive somata and presynaptic dendrites received synapses from at least three varieties of nonimmunoreactive profiles.     

Responses of the reticular nucleus neurons and dorsal thalamic nuclei neurons in the cat during extinction of a conditioned instrumental reflex

Activity of 66 neurons of the reticular nucleus (R), 31 neurons of the ventroposterolateral nucleus and 14 neurons of the posterolateral nucleus-pulvinar complex of the thalamus was investigated during extinction of the conditioned instrumental alimentary reflex. The quantity of R neurons that show initial excitation in response to the conditional stimulus in the first 300 ms decreased during extinction. Conditioned placing reactions and late excitatory and inhibitory neuronal responses in the R and dorsal thalamic nuclei with latency above 300 ms disappeared during extinction simultaneously. The background unit activity decreased during extinction in the 2/3 of investigated neurons of R and dorsal thalamic nuclei. It is suggested that the efferent influence from the R decreased during extinction.     

Cytology and synaptology of the lateral reticular nucleus of the cat

The organization of lateral reticular nucleus (LRN) of the cat was investigated using electron microscopy and Golgi techniques. Golgi-Cox preparations revealed that the LRN consists of allodendritic and, especially, isodendritic neurons. The latter have been associated with neural centres that have important roles integrating signals from distant sources. Several forms of spines were identified with the Golgi method, and their ultrastructural correlates were determined. Somatic spines resembled stubby protrusions, while dendritic spines, where were usually observed on distal dendrites, appeared as pedunculated spines, racemose appendages and spine-crowned appendages. Ultrastructural examination of this nuclease revealed various synaptic relationships. The majority of the synaptic terminals were small (1.5--2.5 micrometer in diameter), contained round vesicles and usually contacted dendrites and spines. Other small terminals contained pleomorphic vesicles and contacted distal dendrites and spines. Large terminals (greater than 2.5 micrometer in diameter) with round or pleomorphic vesicles contacted the somata or proximal dendrites. Three types of "synaptic configurations," which consisted of discrete aggregations of neuronal processes invested by astrocytic lamellae, were also identified. These structural arrangements likely provide a basis for the integration of inputs to the LRN from spinal and supraspinal centres.     

Functional subsets of neurons in somatosensory thalamus of the cat

Functional properties of somatosensory thalamic neurons isolated within a region encompassing nucleus ventralis posterolateralis were studied in chloralose-anesthetized cats. A sample of these neurons responding to electrical stimulation of the contralateral forepaw was reconstructed by pooling data from 46 individual animals on the basis of unit spatial location. Seventy percent of the 640 neurons studied responded only to the contralateral forepaw; they had small receptive fields as determined by natural stimulation, generally on the digits and the dorsum of the paw, and 75% of this group were excited by light touch or deflection of hairs. Thirty percent of the neurons studied responded to the contralateral forepaw and to other limbs as well, their larger receptive fields often being bilateral. Approximately 50% of these wide-field neurons were excited by gentle mechanical stimulation. Some cells of this type were identified as projection neurons by virtue of their antidromic activation from the S I forepaw area of cerebral cortex. The wide-field neurons described here are not adequately explained as vestigial aberrations persisting at the feline stage in an evolutionary trend toward strictly somatotopic thalamic representation. Comparison of the dynamic response properties (latency, spikes per discharge, and frequency-following) of small- and wide-field somatosensory thalamic neurons suggests that they are activated via different input mechanisms and that each has a particular functional role in somesthesis.     

Morphological and physiological identification of excitatory pontine reticular neurons projecting to the cat abducens nucleus and spinal cord

The current study provides strong morphological and physiological evidence for identifying reticular neurons which project to the ipsilateral abducens nucleus. In conjunction with recent work in the alert cat, these neurons are believed to be excitatory and are implicated to play a role in the generation of saccadic and/or vestibular fast phase eye movements.