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A B Karabelas

Publications and source records attributed to A B Karabelas.

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Structure-function relationships in the primate superior colliculus. I. Morphological classification of efferent neurons.

1. Neurons in the superior colliculus (SC) of anesthetized paralyzed squirrel monkeys were injected intracellularly with horseradish peroxidase (HRP) to establish a morphological classification of tectal efferent neurons in this species. These neurons were physiologically identified by their antidromic responses following stimulation of the contralateral predorsal bundle or SC. These cells also responded with postsynaptic potentials to stimulation of the ipsilateral substantia nigra and cerebral peduncle and the contralateral tectum. 2. Quantitative light microscopic analysis of the somatodendritic profiles and axonal trajectories of 27 recovered cells revealed the existence of three major groups of tectal efferent neurons: L (n = 7), X (n = 8), and T (n = 12). 3. L neurons are small or medium size cells with relatively elaborate dendritic trees and are located mainly in the superficial layers of the SC. They participate in the ipsilateral descending and dorsal ascending tectofugal bundles. Intrinsic collaterals of L axons deploy a large number of boutons both near the parent cell body and more ventrally within the deeper tectal layers. 4. X neurons are mostly large in size and multipolar in shape with relatively complex dendritic trees. Their cell bodies are situated mainly in the stratum griseum intermedium and occasionally in the stratum opticum. Axons of X neurons participate in the crossed descending and ipsilateral ventral ascending projections of the SC. In addition, the axonal system of about half of the X neurons includes recurrent collaterals. 5. T neurons are located mainly in the ventral stratum opticum and the dorsal stratum griseum intermedium. They have small or medium-sized, trapezoid or ovoid cell bodies and relatively simple radiating or vertical dendritic trees. Their axons usually participate in two of the major tectofugal bundles besides providing a commissural component and recurrent collaterals. 6. Morphological details revealed in the present study support the notion that distinct tectofugal axonal systems originate from efferent neurons of the primate SC that differ both as to their location in the tectum as well as the appearance of their somata and dendritic trees. The resulting morphological classification of tectal efferent cells provides a framework for the analysis of tectal function in terms of populations of identified neurons.

Animals

Structure-function relationships in the primate superior colliculus. II. Morphological identity of presaccadic neurons.

1. Microelectrodes filled with horseradish peroxidase (HRP) were inserted in the superior colliculus (SC) of alert squirrel monkeys. Spontaneous eye movements were monitored in the dark during recording and intraaxonal injection of fibers carrying presaccadic signals. 2. Analysis of the relationship between neuronal activity and saccadic parameters indicates that saccade-related neurons can be functionally classified into: 1) vectorial long-lead burst neurons (n = 31), and 2) directional long-lead burst neurons. 3. Vectorial long-lead burst neurons have little if any spontaneous activity and burst intensely before spontaneous saccades within their movement fields with a latency of approximately 20 ms. Their cell bodies were recovered mostly (4/5) in the stratum opticum of the SC. The mediolateral and anteroposterior location of these tectal long-lead burst neurons (TLLBs) together with their movement fields are consistent with existing descriptions of the motor map of the deeper tectal layers. Due to their somatodendritic morphology and pattern of axonal trajectories, TLLBs belong to the T group of tectal efferent neurons that was described in our companion report. Through its branched axonal system each TLLB can relay a signal coding intended eye displacement to reticular targets of the predorsal bundle (PDB), contralateral tectum, ipsilateral mesencephalic reticular formation (MRF), and rostrally located ipsilateral targets of the SC, besides participating in intratectal information processing. 4. Recovered tectal neurons (n = 4) with activity not related to spontaneous saccades participate in the predorsal and ventral ascending tectofugal bundles as well as the projection to the ipsilateral mesencephalic reticular formation. They do not participate in the commissural projection of the SC and need not have recurrent collaterals. Due to their somatodendritic morphology and pattern of axonal trajectories, these cells belong to the X group of tectal efferent neurons that was described in the preceding paper. 5. Recovered cells of origin of directional long-lead burst fibers recorded in the SC (n = 5) are located in the tectorecipient portion of the MRF and their axonal terminals are entirely contained within the SC. The high-frequency portion of the discharge of these reticulotectal long-lead burst neurons (RTLLBs) precedes most contraversive saccades by approximately 19 ms.(ABSTRACT TRUNCATED AT 400 WORDS)

Action Potentials

Observations on the somatodendritic morphology and axonal trajectory of intracellularly HRP-labeled efferent neurons located in the deeper layers of the superior colliculus of the cat.

Efferent neurons of the deeper layers of the cat's superior colliculus were stained with horseradish peroxidase (HRP) to demonstrate patterns of somatodendritic morphology and axonal trajectory. A combination of somatodendritic and axonal features of the HRP-labeled cells revealed the existence of three major groups of tectal efferent neurons (X, T, and I). X neurons are mostly large and multipolar and participate in the crossed descending and ipsilateral ventral ascending projections of the superior colliculus. The X group includes multipolar radiating (X1), tufted (X2), large vertical (X3), medium-sized vertical (X4), and medium-sized horizontal (X5) neurons. T neurons participate in one or two of the major tectofugal bundles (medial descending ipsilateral, lateral descending ipsilateral, medial dorsal ascending, crossed descending) besides providing a commissural branch. They also issue recurrent collaterals distributed within a more or less restricted area of the deeper layers. The T group includes medium-sized, trapezoid, radiating (T1) and small or medium-sized, ovoid, vertical (T2) neurons. I neurons participate in the ipsilateral descending projection of the superior colliculus. They are small, triangular or ovoid, sparsely ramified cells that provide long, varicose collaterals irregularly distributed within the deeper layers. The majority of T neurons are located in the ventral stratum opticum or dorsal stratum griseum intermediale; X3 and X5 neurons are situated immediately below in the dorsal stratum griseum intermediale, while X1, X2, X4, and I neurons are indiscriminately distributed within the deeper layers. The polythetic classification presented here provides a conceptual framework for the description of tectal efferent neurons. It is open-ended and can thereby accommodate new cells types as indicated by the disclosure of a small horizontal (A) and a small radiating (unclassified) neuron. Moreover, it does not preclude the construction of alternate taxonomies. A dendro-architectonic classification into four groups [vertical (X3, X4, T2, I), horizontal (X5, A), radiating (X1, T1, I), and tufted (X2)] can be made and would relate to the mode of integration of various tectopetal inputs. A classification based on the dorsoventral location of tectal efferent neurons is also possible and would relate to the dorsoventral distribution of neurons with specific response properties.

Animals

Nigral inhibitory termination on efferent neurons of the superior colliculus: an intracellular horseradish peroxidase study in the cat.

Intracellularly recorded responses of deeper tectal neurons to stimulation of the substantia nigra and the cerebral peduncle were obtained to demonstrate the monosynaptic inhibitory nature of the nigrotectal pathway in the cat. We also employed antidromic stimulation (contralateral predorsal bundle and superior colliculus) and intracellular labeling with HRP to demonstrate which types of tectal efferent neurons are nigrorecipient. The response to nigral stimulation in 61% of the cells studied was a monosynaptic IPSP of short duration. Recovered HRP-labeled nigrorecipient neurons include X1 (large multipolar radiating), X2 (tufted), X4 (medium-size vertical), X5 (medium-size horizontal), T1 (medium-size trapezoid radiating), T2 (small ovoid vertical), I (small sparsely ramified), and A (small horizontal) neurons. Nigrorecipient cells participate in all four of the major efferent axonal systems of the deeper tectal layers: crossed descending (X and T neurons), ipsilateral descending (I and T neurons), ascending (A, X, and T neurons), and commissural (T neurons). EPSPs accompanied by long-lasting hyperpolarizing potentials were recorded from the remaining tectal neurons in response to stimulation of the substantia nigra, cerebral peduncle, and pericruciate cortex. Collision experiments indicate that at least part of the excitatory responses of tectal neurons to nigral and penduncular stimulation are mediated by corticotectal fibers traversing the cerebral peduncle and the substantia nigra. Excitatory effects of nigral, peduncular, and cortical stimulation were disclosed in X neurons including the non-nigrorecipient large vertical neurons of the X3 subgroup. Cortical excitatory and nigral inhibitory inputs converge only on X neurons (X1, X2, X4, X5). In this case, nigrally evoked IPSPs were preceded by a brief EPSP. Collectively, these results demonstrate the inhibitory termination of the nigrotectal pathway on a wide variety of deeper tectal efferent neurons. Such findings imply the versatility of the nigral involvement in tectal mechanisms of gaze control. We suggest that the substantia nigra pars reticulata contacts tectal neurons differing as to their response properties and shapes the signal carried by all the major tectofugal bundles.

Animals

Altered patterns of evoked synaptic activity in cortical pyramidal neurons in feline ganglioside storage disease.

Postsynaptic potentials evoked by ventrolateral thalamic stimulation were recorded intracellularly from neurons in the precruciate cortex of GM1 mutants with HRP- or LY-loaded microelectrodes. Ganglioside-laden pyramidal neurons exhibiting somal distention and/or meganeurite formation were found to respond to thalamic stimulation with short duration IPSPs. Evoked EPSPs were recorded from two morphologically characterized large basket intrinsic neurons which deployed extensive intracortical axonal arborizations. These findings point to the preservation of intracortical inhibitory networks in the feline model of GM1 gangliosidosis, and to the possibility of abnormal integration of somadendritic inputs in ganglioside-laden pyramidal neurons.

Animals