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S M Sherman

Publications and source records attributed to S M Sherman.

At least 19 recordsLinked to original sources

Effects of membrane voltage on receptive field properties of lateral geniculate neurons in the cat: contributions of the low-threshold Ca2+ conductance.

1. Thalamic relay cells, including those of the lateral geniculate nucleus, display a low-threshold spike (LT spike), which is a large depolarization due to an increased Ca2+ conductance. Typically riding the crest of each LT spike is a burst of from two to seven action potentials, which we refer to as the LT burst. The LT spike is voltage dependent, because if the cell's resting membrane potential is more depolarized than roughly -60 mV, the LT spike is inactivated, but if more hyperpolarized, the spike is deinactivated and can be activated by a depolarization, such as from an afferent excitatory postsynaptic potential (EPSP). Thalamic relay cells thus display two response modes: a relay or tonic mode, when the cell is depolarized and LT spikes are inactivated, leading to tonic firing of action potentials; and a burst mode, when the cell is hyperpolarized and tends to respond with LT spikes and their associated bursts of action potentials. 2. We were interested in the contribution of the LT spike on the transmission of visually evoked signals through geniculate relay cells to visual cortex. We recorded intracellularly from geniculate cells in an anesthetized, paralyzed, in vivo cat preparation to study the effects of membrane voltage, and thus the presence or absence of LT spikes, on responses to drifting sine-wave gratings. We monitored the visually evoked responses of 14 geniculate neurons (6 X, 7 Y, and 1 unclassified) at different membrane potentials at which LT spikes were inactivated or deinactivated. 3. Changing membrane voltage during visual stimulation switched the response mode of every cell between the relay and burst modes. In the burst mode, LT spikes occurred in phase with the visual stimulus and not at rhythmic intervals uncorrelated to visual stimuli. To any given stimulus cycle, the cell responded usually with an LT burst or a tonic response, and rarely was more than one LT burst evoked by a stimulus cycle. Occasionally a single cycle evoked both an LT burst and tonic response, but always the LT burst occurred first. 4. The spatial tuning characteristics of the cells did not differ dramatically as a function of membrane potential, because the tuning of the LT bursts was quite similar to that of the tonic response component. Although we did not obtain complete temporal tuning properties, we did note that hyperpolarized cells responded reliably with LT bursts at several temporal frequencies. 5. A consistent difference was seen between the LT burst and tonic response components in terms of response linearity.(ABSTRACT TRUNCATED AT 400 WORDS)

Action Potentials

Relative contributions of burst and tonic responses to the receptive field properties of lateral geniculate neurons in the cat.

1. In an anesthetized, paralyzed in vivo preparation, we recorded extracellular responses of 61 geniculate neurons (2 W, 25 X, 33 Y, and 1 mixed) to drifting sine-wave gratings of various spatial frequency, temporal frequency, and contrast. Our goal was to study the differential contributions to these visual responses of bursting caused by voltage dependent, low-threshold (LT) Ca2+ spikes and of purely tonic responses unrelated to LT spikes. Cells responding with LT spikes are said to be in the burst firing mode and those responding in a purely tonic fashion to be in the relay or tonic firing mode. We separated the total visual response into LT burst and tonic components by use of the empirical criteria set forth in our intracellular study described in the previous paper (Lu et al. 1992). A response component was considered to be an LT burst if its action potentials displayed interspike intervals < or = 4 ms and if the first spike in the burst episode occurred after a silent period of > or = 100 ms (or > or = 50 ms when the neuron responds to visual stimuli at temporal rates > or = 8 Hz). All other activity is considered to be part of the tonic response. 2. In addition to LT bursts, we recognized another type of burst response, the high-threshold (HT) burst. These also have clusters of action potentials with interspike intervals < or = 4 ms. However, HT bursts, unlike LT bursts, lack a preburst silent period. HT bursts are part of the tonic response component and merely reflect the gradual decrease in interspike intervals that occurs as the cell becomes more depolarized and thus more responsive. Thus interspike interval is a necessary but insufficient criterion to identify LT bursts. 3. Visually evoked LT bursts were recorded among W, X, and Y cells. When evoked, LT bursts occurred in phase with drifting sine-wave grating stimuli at a rate never exceeding one per stimulus cycle. In response to individual cycles of the visual stimulus, LT bursts could comprise the total response, a tonic component could comprise the total response, or an LT burst and tonic component could be mixed. When a stimulus evoked a mixture of LT bursts and tonic response components, LT bursts were always the first response. 4. Of the 61 cells tested with grating stimuli, 47 exhibited LT bursts and 14 did not. Those that did exhibited varying amounts of burstiness.(ABSTRACT TRUNCATED AT 400 WORDS)

Action Potentials

Electron-microscopic analysis of synaptic input from the perigeniculate nucleus to the A-laminae of the lateral geniculate nucleus in cats.

The perigeniculate nucleus of carnivores is thought to be a part of the thalamic reticular nucleus related to visual centers of the thalamus. Physiological studies show that perigeniculate neurons, which are primarily GABAergic, provide feedback inhibition onto neurons in the lateral geniculate nucleus. However, little is known about the anatomical organization of this feedback pathway. To address this, we used two complementary tracing methods to label perigeniculate axons for electron microscopic study in the geniculate A-laminae: intracellular injection of horseradish peroxidase (HRP) to fill an individual perigeniculate cell and its axon; and anterograde transport of Phaseolus vulgaris leucoagglutinin to label a population of perigeniculate axons. Labeled perigeniculate terminals display features of F1 terminals in the geniculate neuropil: they are small, contain dark mitochondria, and form symmetric synaptic contacts. We found that most of the perigeniculate terminals (greater than 90%) contact geniculate cell dendrites in regions that also receive a rich innervation from terminals deriving from visual cortex (e.g., "cortico-recipient" dendrites). The remainder of the perigeniculate synapses (10%) contacted dendrites in regions that also received direct retinal input (e.g., "retino-recipient" dendrites). Serial reconstruction of segments of dendrites postsynaptic to perigeniculate terminals suggests that these terminals contact both classes of relay cell in the A-laminae (X and Y), although our preliminary conclusion is that an individual perigeniculate cell contacts only one class. Finally, our quantitative comparison between labeled perigeniculate terminals and unlabeled F1 terminals indicates that these perigeniculate terminals form a distinct subset of F1 terminals. We quantitatively compared the labeled perigeniculate terminals to unlabeled F1 terminals. Although the parameters of the perigeniculate terminals fell entirely within the range of those for the unlabeled F1 terminals, as populations, we found consistent differences between these two groups. We thus conclude that, as populations, other sources of F1 terminals are morphologically distinct from perigeniculate terminals and innervate different targets.

Animals

Intracellular and extracellular in vivo recording of different response modes for relay cells of the cat's lateral geniculate nucleus.

Prior studies of thalamic neurons have demonstrated that they exhibit at least two response modes: a relay mode and a burst mode. During the relay mode, sensory information is faithfully relayed to cortex; during the burst mode, which is caused by a voltage-dependent Ca2+ conductance, this relay of sensory information is interrupted. We began in vivo studies of these response modes in neurons from the lateral geniculate nucleus of anesthetized, paralyzed cats. Each of the 9 X and 10 Y cells we recorded intracellularly displayed voltage-dependent, low threshold spikes that were presumably the Ca2+ spikes described from in vitro recording. These spikes were triangular in waveform and typically had 2-7 fast action potentials (interspike intervals of 1.2-4 ms) riding its crest. Furthermore, the cell's membrane had to be hyperpolarized to de-inactivate the low threshold spike before a depolarization could then activate it. We could activate these low threshold spikes in Y cells from EPSPs, whether spontaneous or evoked from activation of the optic chiasm. However, in only one of the X cells could we activate low threshold spikes from chiasm shock; in the remainder, we could activate low threshold spikes only via depolarizing current pulses, possibly because the EPSPs of these X cells were too small to activate these spikes. We also used extracellular recording to study spontaneous activity and responses to chiasm shock from 114 geniculate neurons and, as a control, 57 optic tract axons. We concentrated on periods of bursty responsiveness signifying the burst mode. We define a burst as 2-7 action potentials with interspike intervals less than or equal to 4 ms, and the bursts are separated by greater than 100 ms; from our intracellular recording, we know that such bursts signify low threshold spikes. We found that, during extracellular recording, 20 of the 39 X cells and each of the 75 Y cells displayed evidence of the burst response mode, although burst periods were rare in X cells. Electrical activation of the optic chiasm greatly enhanced the burstiness of Y cells for periods of 500 ms or more. We also electrically stimulated the parabrachial region of the midbrain, which provides a mostly cholinergic innervation to the lateral geniculate nucleus. Although parabrachial activation by itself had no detectable effect on Y cell response modes, prior parabrachial activation prevented the enhanced burstiness caused by chiasm stimulation. This parabrachial effect lasted for roughly 500 ms after stimulation.(ABSTRACT TRUNCATED AT 400 WORDS)

Action Potentials

A GABAergic projection from the pretectum to the dorsal lateral geniculate nucleus in the cat.

To study the projection from the pretectum to the lateral geniculate nucleus, we placed wheat-germ agglutinin conjugated to horseradish peroxidase into the lateral geniculate nuclei of six cats, allowed this marker to be retrogradely transported by afferent axons to their parent somata in the pretectum, and revealed the label in these cells with stabilized tetramethylbenzidine histochemistry. In three cases we made large pressure injections that completely infiltrated the lateral geniculate nucleus and extended into neighboring thalamic nuclei; in the other three we made smaller iontophoretic injections largely confined to the A- and C-laminae of the lateral geniculate nucleus. In both types of injection we found labeled pretectal cells mainly in the nucleus of the optic tract but also found some cells labeled in the olivary pretectal nucleus and the posterior pretectal nucleus. After one of the larger injections we analysed both sides of the pretectum and found that 11% of the labeled cells were located contralaterally and were distributed in the same three nuclei. We analysed only the ipsilateral side in the remaining five cats. In those five experiments we also immunohistochemically stained the pretectal sections with an antibody directed against the neurotransmitter, GABA. Of the retrogradely labeled pretectal cells, 40% were also labeled for GABA, and those were similar in soma size (350 microns 2 in cross-sectional area) to those labeled only with the retrograde marker (331 microns 2). GABA-positive cells not labeled by retrograde transport were smaller (246 microns 2) than either of these other cells populations. These results indicate that at least 40% of the cells involved in the projection from the pretectum to the lateral geniculate nucleus are GABAergic. We suggest that this extrathalamic projection may serve to inhibit thalamic GABAergic cells. This, in turn, would disinhibit geniculate relay cells, thereby facilitating the geniculate relay of retinal information to cortex.

Afferent Pathways

Morphology and axonal projection patterns of individual neurons in the cat perigeniculate nucleus.

1. The lateral geniculate nucleus is the primary thalamic relay through which retinal signals pass en route to cortex. This relay is gated and can be suppressed by activity among local inhibitory neurons that use gamma-aminobutyric acid (GABA) as a neurotransmitter. In the cat, a major source of this GABAergic inhibition seems to arise from cells of the perigeniculate nucleus, which lies just dorsal to the A-laminae of the lateral geniculate nucleus. However, the morphological characteristics of perigeniculate cells, and particularly the projection patterns of their axons, have never been fully characterized. We thus examined the morphology of these cells: individually by intracellular injection of horseradish peroxidase (HRP) and en masse with the anterograde tracer Phaseolus vulgaris leucoagglutinin (PHAL). 2. We recorded from 12 perigeniculate cells that we impaled and successfully labeled with HRP. These cells exhibited response properties generally consistent with those described previously. They had long response latencies to stimulation of the optic chiasm and relatively large, often diffuse, receptive fields. The visually evoked responses of most of the cells were dominated by one eye. Compared with cells of the lateral geniculate nucleus, perigeniculate cells had large somata (517 +/- 136 microns 2 in cross-sectional area, mean +/- SD), which were fusiform or multipolar in shape, and dendritic arbors that extended a considerable distance (1,095 +/- 167 microns) parallel to the border between the perigeniculate and lateral geniculate nuclei. Terminal arbors of some dendrites were quite complex and beaded. 3. The axons of six perigeniculate cells were labeled sufficiently well to trace and reconstruct over a considerable distance. Each of these axons formed branches that descended to innervate the lateral geniculate nucleus, and this geniculate innervation was exclusively limited to the A-laminae. Terminal boutons within the A-laminae were nearly all en passant, which gave the axons a beaded appearance. Furthermore, branches of five of these six axons provided local innervation of the perigeniculate nucleus, generally within each labeled cell's own dendritic arbor. Three of the cells also exhibited an axon branch that extended medially and caudally away from the soma, but we were unable to trace these axon branches to their targets. 4. Within the lateral geniculate nucleus, each arbor of perigeniculate axons derived from two main components. One was a narrow, sparse medial component that innervated laminae A and A1.(ABSTRACT TRUNCATED AT 400 WORDS)

Animals

In vivo recording of postsynaptic potentials and low threshold spikes in W cells of the cat's lateral geniculate nucleus.

We obtained good intracellular recording from 5 W cells in the C-laminae of the cat's lateral geniculate nucleus. The recordings were made from an anesthetized and paralyzed in vivo preparation. We found a consistent pattern for the postsynaptic potentials evoked from activation of the optic chiasm: first was an IPSP followed by an EPSP. This is very different from the pattern seen in X and Y cells, for which an EPSP always appears first and is then followed by an IPSP. We interpret the pattern for W cells as follows. The initial IPSP is disynaptic; this involves retinogeniculate conduction over very fast Y axons and a relay through an interneuron. The EPSP is monosynaptic, reflecting retinogeniculate conduction over very slow W axons. A possible implication for this is that activity over the Y pathway may generally inhibit geniculate W cells before these W cells can be excited by their retinal afferents. Finally, we elicited from each of these W cells voltage-dependent, low threshold spikes, which are very similar to those displayed by X and Y cells. These spikes can interrupt normal retinogeniculate transmission, and they are prevented by maintaining relatively depolarized membrane potentials.

Animals

N-methyl-D-aspartate receptors contribute to excitatory postsynaptic potentials of cat lateral geniculate neurons recorded in thalamic slices.

Neurons of the cat's dorsal lateral geniculate nucleus were recorded intracellularly to study the contribution of N-methyl-D-aspartate (NMDA) receptors to excitatory postsynaptic potentials (EPSPs) and low-threshold calcium spikes. EPSPs were evoked by stimulation of retinogeniculate axons in the optic tract and/or corticogeniculate axons in the optic radiations; EPSPs from both sources were similar. These EPSPs had one or two components, and the second component had several characteristics of NMDA receptor-mediated events. For example, EPSP amplitude decreased when neurons were hyperpolarized and increased when stimulus frequency was increased; these EPSPs could also be blocked reversibly by application of the selective NMDA receptor antagonist DL-2-amino-5-phosphonovaleric acid (APV). We also studied the influence of NMDA receptors on low-threshold calcium spikes, which are large, voltage- and calcium-dependent depolarizations that are often accompanied by high-frequency action potential discharge. APV blocked synaptically activated low-threshold calcium spikes, but APV had no effect on low-threshold calcium spikes that were elicited by current injection. Therefore, APV does not appear to have a direct effect on the T-type calcium channel that is involved in generation of low-threshold calcium spikes. The voltage and frequency dependence of the NMDA receptor-mediated component of the EPSPs, as well as its ability to trigger low-threshold calcium spikes, provide for complex signal processing in the lateral geniculate nucleus.

2-Amino-5-phosphonovalerate

Brainstem control of response modes in neurons of the cat's lateral geniculate nucleus.

The visual pathway from retina through the lateral geniculate nucleus to visual cortex in the cat is comprised of several parallel neuronal streams that independently analyze different aspects of the visual scene. The best known of these are the X and Y pathways that relay through the geniculate A laminae. Recent receptive-field studies of retinal and geniculate neurons suggest that there is a further elaboration of cell types at the level of the lateral geniculate nucleus. That is, two types of geniculate X cells with different temporal patterns of responses to visual stimuli are recognized, one with "nonlagged" features, exhibiting shorter response latencies and another with "lagged" features; all retinal X cells are nonlagged. We asked whether nonlagged and lagged responses represent different cell classes or two response modes of the same cells, perhaps under the control of nonretinal afferents to these relay cells. Accordingly, we studied the effects on appropriate receptive-field properties of electrical activation of the midbrain parabrachial region, which is a major nonretinal input to relay cells. Such parabrachial stimulation made each of the eight lagged X cells much more like nonlagged cells, and this stimulation completely transformed the lagged response profiles of six of the eight cells to nonlagged. We thus conclude that the property of lagged responsiveness, which is an emergent property of the lateral geniculate nucleus, is a different response mode of the same cells that can also display nonlagged responses, rather than representing different cell classes; furthermore, this switching between response modes is, at least partly, under the control of afferents from the parabrachial region.

Animals

Dendritic current flow in relay cells and interneurons of the cat's lateral geniculate nucleus.

We used a passive, steady-state cable model to simulate current flow within the dendritic arbors of relay cells and interneurons in the cat's lateral geniculate nucleus. In confirmation of our previous work on relay cells, we found them to be electronically compact; thus a postsynaptic potential generated anywhere in a relay cell's dendritic arbor spreads with relatively little attenuation throughout the arbor and to its soma. An interneuron is very different. Its arbor is much more extensive electronically with the result that a postsynaptic potential significantly affects only local areas of the dendritic arbor, and only inputs to proximal dendrites or to the soma will much affect the soma. Since much of the interneuron's synaptic output derives from dendritic terminals that are both presynaptic and postsynaptic, its dendritic arbor may contain many local circuits that perform neuronal computations independently of each other, and this processing might be invisible to the soma. Furthermore, these interneurons possess conventional axonal outputs, and these contact postsynaptic profiles that are quite different from the postsynaptic targets of the dendritic terminals. Presumably, the axonal output reflects the integrated computations performed on proximal synaptic inputs, and it uses conventional action potentials to convey this output. We suggest that the interneuron does double duty: its dendritic arbor is used for many independent local circuits that perform one set of neuronal computations, and its axonal output represents conventional neuronal integration of proximal synaptic inputs.

Animals

Identification of X versus Y properties for interneurons in the A-laminae of the cat's lateral geniculate nucleus.

Roughly 25% of the neurons in the A-laminae of the cat's lateral geniculate nucleus are local interneurons, while the remaining 75% are relay cells that project to the visual cortex. The interneurons form the focus of our study. The relay cells are either X or Y cells and are thereby integral links in the parallel and independent retino-geniculo-cortical X and Y pathways. Little is known about the response properties of interneurons, largely because it is difficult to identify them clearly during electrophysiological recording. However, they can be identified by morphological criteria. We thus studied their response properties by recording intracellularly from geniculate neurons to characterize them and then injecting them with horseradish peroxidase (HRP); the HRP labeling subsequently allowed us to distinguish relay cells from interneurons. In this manner, we studied 171 relay cells (83 X and 88 Y) and 15 interneurons. The response properties tested for each of the interneurons were indistinguishable from those of the relay X cells. We conclude that these interneurons are directly innervated by retinogeniculate X axons and are firmly embedded in the X pathway. We found no evidence for interneurons in the Y pathway.

Action Potentials

Postsynaptic potentials recorded in neurons of the cat's lateral geniculate nucleus following electrical stimulation of the optic chiasm.

1. We recorded intracellularly from X and Y cells of the cat's lateral geniculate nucleus and measured the postsynaptic potentials (PSPs) evoked from electrical stimulation of the optic chiasm. We used an in vivo preparation and computer averaged the PSPs to enhance their signal-to-noise ratio. 2. The vast majority (46 of 50) of our sample of X and Y cells responded to stimulation of the optic chiasm with an excitatory postsynaptic potential (EPSP) followed by an inhibitory postsynaptic potential (IPSP); these were tentatively identified as relay cells. We quantified several parameters of these PSPs, including amplitude, latency, time to peak (i.e., rise time), and duration. 3. Among the relay cells, the latencies of both the EPSP and action potential evoked by optic chiasm stimulation were shorter in Y cells than in X cells. Furthermore, the difference between the latencies of the EPSP and action potential was shorter for Y cells than for X cells. This means that the EPSPs generated in Y cells reached threshold for generation of action potentials faster than did those in X cells. The EPSPs of Y cells also displayed larger amplitudes and faster rise times than did those in X cells, but neither of these distinctions was sufficient to explain the shorter latency difference between the EPSP and action potential for Y cells. 4. The EPSPs recorded in relay Y cells had longer durations than did those in relay X cells. Our data suggest that the subsequent IPSP actively terminates the EPSP, which, in turn, suggests that the time interval between EPSP and IPSP onsets is longer in Y cells than in X cells. Furthermore, we found that, for individual Y cells, the latency and duration of the evoked EPSP were inversely related. These observations lead to the conclusion that the latency of IPSPs activated from the optic chiasm is relatively constant among Y cells and thus independent of the EPSP latencies. Thus the excitation and inhibition produced in individual geniculate Y cells may originate from different populations of retinogeniculate axons. 5. The IPSPs recorded in geniculate relay cells following optic chiasm stimulation could be divided into three groups based on their durations. The majority of both X and Y cells showed short-duration IPSPs, whereas the remainder of Y cells displayed medium-duration IPSPs, and the remaining X cells displayed long-duration IPSPs. A positive correlation was seen between the time to peak and duration of these IPSPs.(ABSTRACT TRUNCATED AT 400 WORDS)

Animals

Morphology of retinogeniculate X and Y axon arbors in cats raised with binocular lid suture.

1. We examined the terminal arbors of single, physiologically identified retinogeniculate X and Y axons in 13 adult cats raised from birth with binocular lid suture. We recorded in the optic tract from 146 retinogeniculate axons. We studied the response properties of each axon encountered and attempted to penetrate it for labeling with horseradish peroxidase. 2. We attempted to classify each retinogeniculate axon as X or Y on a standard battery of tests. We thus identified 46 X and 91 Y axons; 5 axons had unusual response properties, and 4 axons were lost before they could be adequately identified. The X and Y axons had response properties that were completely normal by our criteria. The 5 unusual axons exhibited linear spatial and temporal summation, which is a property of X cells, despite all of their other tested response properties being consistent with those of Y cells. 3. We achieved complete, dark labeling of 13 X and 13 Y axons that form the data base for all of our qualitative and quantitative morphological observations. All of these labeled axons had response properties entirely normal for their X or Y class. Nine of the labeled X axons arise from the contralateral retina and 4 from the ipsilateral retina, whereas the respective numbers for the Y axons are 8 and 5. 4. Each of the individual retinogeniculate X axons form terminal arbors that appeared essentially normal in terms of location within geniculate lamina A or A1, shape, volume, and number of terminal boutons. 5. In contrast, the retinogeniculate Y axons form clearly abnormal arbors with diminished projections, both in terms of bouton numbers and arbor volumes. For Y axons from the contralateral retina, a roughly normal arbor is formed in the C-laminae, despite greatly diminished or absent projections formed in lamina A, something never seen in normal cats. For Y axons from the ipsilateral retina, the projections to lamina A1 are also diminished, and the arbors there are all limited to the ventral half of the lamina, a pattern rarely seen for normal Y axons. 6. The selective reduction in retinogeniculate Y axon arbors in these binocularly lid-sutured cats is consistent with similar observations reported for monocularly lid-sutured and strabismic cats but is quite different from the apparently normal development of retinogeniculate axon arbors in cats raised in complete darkness.(ABSTRACT TRUNCATED AT 400 WORDS)

Animals

The projection of individual axons from the parabrachial region of the brain stem to the dorsal lateral geniculate nucleus in the cat.

In mammals, the retinogeniculocortical pathway is the primary afferent route to visual cortex. The flow of information along this pathway can be modulated at the thalamic level (i.e., at the lateral geniculate nucleus) as a function of arousal, attention, and phenomena such as eye movements. Physiological studies indicate that an important source of this state-dependent influence on geniculate neuronal responsiveness is the parabrachial region of the brain stem. We used the anterograde tracer Phaseolus vulgaris leucoagglutinin to study the anatomical connections between the parabrachial region and the lateral geniculate nucleus. Labeled parabrachial axons are found throughout the thalamus, including all laminae of the lateral geniculate nucleus, the lateral posterior-pulvinar complex, the ventral lateral geniculate nucleus, the perigeniculate nucleus, and the reticular nucleus of the thalamus. Within these nuclei, the axons exhibit sporadically branched terminal arbors with boutons mostly en passant. Serial reconstructions indicate that individual parabrachial axons that innervate the lateral geniculate nucleus may terminate in other visual thalamic nuclei as well, but not in thalamic nuclei that subserve other modalities. Finally, the labeled parabrachial axons are morphologically heterogeneous; they differ in their innervation targets, terminal arbor shape, and the size spectrum of their boutons. These data suggest that this portion of the ascending parabrachial pathway, which may be functionally diverse, coordinates the responsiveness of the varied thalamic nuclei involved with vision.

Animals

Parabrachial innervation of the cat's dorsal lateral geniculate nucleus: an electron microscopic study using the tracer Phaseolus vulgaris leucoagglutinin (PHA-L).

Ascending pathways from the brain stem play a key role, generally facilitatory, in controlling the transmission of retinal information through the lateral geniculate nucleus to the visual cortex (for reviews, see Singer, 1977; Burke and Cole, 1978; Sherman and Koch, 1986). In order to characterize the morphological basis of this brain-stem control, we used the electron microscope to study synaptic terminals labeled anterogradely from injections of the tracer Phaseolus vulgaris leucoagglutinin into the parabrachial region of the brain stem. The labeled axons, which are fine and unmyelinated in our material, form conventional synaptic contacts onto both relay cells and interneurons. These connections are surprisingly selective for certain postsynaptic elements such as the dendritic shafts and appendages of relay cells and the presynaptic dendritic terminals of interneurons. That is, the morphology of contacts made from parabrachial axons varies with the specific postsynaptic profile. Even a single axon can form symmetrical contacts onto F2 terminals, which are synaptic terminals deriving from dendrites of interneurons, and dendritic shafts of relay X cells, and form asymmetrical contacts onto dendritic appendages of the same relay X cells. Reconstructions of the dendritic segments postsynaptic to the labeled terminals show that the dendritic appendages receive retinal and parabrachial input in triadic relationships with F2 terminals: a retinal or parabrachial axon contacts the F2 terminal, and the F2 terminal plus the retinal or parabrachial axon contact the dendritic appendage. This positioning of the parabrachial innervation is well suited for control of retinal transmission. Finally, the dual morphology of the parabrachial synaptic contacts suggests that their actions may differ depending on the postsynaptic target.

Animals

Synaptic circuitry of physiologically identified W-cells in the cat's dorsal lateral geniculate nucleus.

The cat's retinogeniculocortical system is comprised of at least 3 parallel pathways, the W-, X-, and Y-cell pathways. Prior studies, particularly at the level of the lateral geniculate nucleus, have focused on X- and Y-cells. In the present study, we describe the synaptic inputs for 2 geniculate W-cells from the parvocellular C-laminae after these neurons were physiologically identified and intracellularly labeled with HRP. For each of the W-cells, we examined electron micrographs taken from over 500 consecutive thin sections; we reconstructed the entire soma plus roughly 15% of the dendritic arbor and determined the pattern of synaptic inputs to these reconstructed regions of each neuron. In several ways, each W-cell exhibits a similar pattern of synaptic inputs. First, we estimate that each W-cell receives approximately 3000-4000 synaptic contacts, which occur most densely on dendrites 50-150 microns from each soma. Second, axosomatic contacts are extremely rare, and most derive from terminals with flattened or pleomorphic vesicles (F terminals). Third, terminals with round vesicles, large profiles, and pale mitochondria (RLP terminals), which are presumed to be retinal terminals, form only about 2-4% of all synapses onto these W-cells; these synapses occur on proximal dendrites. Fourth, F terminals, which provide roughly 15-20% of all synaptic input to these cells, occupy the same region of proximal dendritic arbor as do the RLP terminals. Fifth, and finally, terminals with round vesicles, small profiles, and dark mitochondria (RSD terminals) provide the majority of synapses along all portions of the dendritic arbor. Compared with geniculate X- and Y-cells of the A-laminae (Wilson et al., 1984), these W-cells are innervated by fewer synapses overall and, in particular, by dramatically fewer synapses from RLP (or retinal) terminals. This paucity of direct retinal input to geniculate W-cells might explain the remarkably poor responsiveness of these neurons to visual stimuli and to electrical activation of the optic chiasm.

Animals

Synaptic circuits involving an individual retinogeniculate axon in the cat.

In order to describe the circuitry of a single retinal X-cell axon in the lateral geniculate nucleus, we physiologically characterized such an axon in the optic tract and injected it intra-axonally with horseradish peroxidase. Subsequently, we recovered the axon and employed electron microscopic techniques to examine the distribution of synapses from 18% of its labeled terminals by reconstructing the unlabeled postsynaptic neurons through a series of 1,200 consecutive thin sections. We found remarkable selectivity for the axon's output, since only four of the 43 available neurons in a limited portion of the terminal arbor receive synapses from labeled terminals. Moreover, the distribution of these synapses on the four neurons, which we term cells 1 through 4, varies with respect to synapses from other classes of terminals that contact the same cells, including synapses from unlabeled retinal terminals. For cells 1 and 3, the labeled terminals provide 49% and 33%, respectively, of their retinal synapses, and these are located on both dendritic shafts and appendages. Synapses from the injected axon to these cells are thus integrated with those from other retinal axons. For cell 2, the labeled terminals provide 100% of its retinal synapses, but these synapses converge on clusters of dendritic appendages where they are integrated with convergent inhibitory inputs. Finally, for cell 4, the labeled terminals provide less than 2% of its retinal inputs, and these are distally located; we suggest that these synapses are remnants of physiologically inappropriate miswiring that occurs during development. The findings from this study support a concept of selectivity in neuronal circuitry in the mammalian central nervous system and also reveal some of the diverse integrative properties of neurons in the lateral geniculate nucleus.

Animals

Passive cable properties and morphological correlates of neurones in the lateral geniculate nucleus of the cat.

1. We used an in vivo preparation of the cat to study the passive cable properties of sixteen X and twelve Y cells in the lateral geniculate nucleus. Cells were modelled as equivalent cylinders according to Rall's formulations (Rall, 1959a, 1969, 1977). We injected intracellular current pulses into these geniculate neurones, and we analysed the resulting voltage transients to obtain the cable parameters of these cells. In addition, fifty-four physiologically characterized neurones were labelled with horseradish peroxidase (HRP) and analysed morphologically. 2. Analysis of HRP-labelled geniculate neurones showed that the dendritic branching pattern of these cells adheres closely to the 3/2 power rule. That is, at each branch point, the diameter of the parent branch raised to the 3/2 power equals the sum of the diameters of the daughter dendrites after each is raised to the 3/2 power. Furthermore, preliminary data indicate that the dendritic terminations emanating from each primary dendrite occur at the same electrotonic distance from the soma. These observations suggest that both X and Y cells meet the geometric constraints necessary for reduction of their dendritic arbors into equivalent cylinders. 3. We found a strong linear relationship between the diameter of each primary dendrite and the membrane surface area of the arbor emanating from it. We used this relationship to derive an algorithm for determining the total somatic and dendritic membrane surface area of an X and Y cell simply from knowledge of the diameters of its soma and primary dendrites. 4. Both geniculate X and Y cells display current-voltage relationships that were linear within +/- 20 mV of the resting membrane potential. This meant that we could easily remain within the linear voltage range during the voltage transient analyses. 5. X and Y cells clearly differ in terms of many of their electrical properties, including input resistance, membrane time constant and electrotonic length. The difference in input resistance between X and Y cells cannot be attributed solely to the smaller average size of X cells, but it also reflects a higher specific membrane resistance (Rm) of the X cells. Furthermore, X cells exhibit electrotonic lengths slightly larger than those of Y cells, but both neuronal types display electrotonic lengths of roughly 1. This indicates that even the most distally located innervation to these cells should have considerable influence on their somatic and axonal responses.(ABSTRACT TRUNCATED AT 400 WORDS)

Action Potentials