Yonago Acta medica 1999;42:163–166

Location of Thalamic Neurons Mediating Vestibulo-Cortical Pathways
in Cats
Satoshi Matsuo, Hiromi Takeuchi, Hisaaki Ikoma and Masae Hosogai*
Department of Oto-Rhino-Laryngology and *Second Department of Physiology, Faculty ofMedicine, Tottori University, Yonago 683-0826, Japan
This study was aimed at examining vestibulo-thalamo-cortical pathways in anesthetizedcats. Thirty-six neurons, which were activated by pitch rotation and contralateral labyrinth stimulation, were recorded in the following areas: the ventral posterolateral nucleus, the ventral posteromedial nucleus, the lateroposterior nucleus and the magnocellular nucleus of the medial geniculate body (MGmc) of the thalamus. Thirteen ofthese neurons were antidromically activated from the anterior suprasylvian sulcus or
postcruciate dimple of the cortex. These results suggest that the ventrobasal complex andMGmc convey inputs from the vestibular apparatus to the vestibular cortex in cats.
Key words: anterior suprasylvian sulcus; cat; postcruciate dimple; posterior semicircular canal;thalamusMany studies have revealed the projection ofneurons in the vestibular nucleus to the thalamus(Landgren et al., 1967; Sans et al., 1970; Ödkvistet al., 1975). Anatomical studies have shownthat thalamic projections to the anterior suprasylvian sulcus (ASSS) and the postcruciate
dimple (PCD) of the cortex originate from theventrobasal complex or magnocellular nucleusof the medial geniculate body (MGmc) (Liedgrenet al., 1976; Mergner et al., 1981). The ASSSand PCD have been identified as receiving vestibular inputs with contralateral dominance incats using the evoked potential technique(Landgren et al., 1967; Sans et al., 1970; Ödkvistet al., 1975). The ASSS also receives inputs
from muscle spindles and the PCD receives inputs from joint receptors (Landgren et al., 1967;Sans et al., 1970; Ödkvist et al., 1975). Thus,
the common feature of these cortical areas is theconvergence of vestibular inputs and signals
from deep somatic receptors (Landgren et al.,
1967; Sans et al., 1970; Ödkvist et al., 1975;
Liedgren et al., 1976; Mergner et al., 1981).
We have reported that axons of posterior
canal (PC)-activated secondary excitatory ves-

tibular neurons project to the oculomotor nucleus, and give off axon collaterals to the thalamus, particularly to the ventrobasal complex
in cats (Matsuo et al., 1994). However, thephysiological feature of the connection between
the PC neurons and the thalamus has beenpractically unknown. That is, it is uncertain
whether axons of the PC neurons make excitatory synapses with the thalamic neurons or are
only passing fibers in the thalami. Furthermore,
no firing pattern or precise location of thethalamic neurons mediating the vestibulocortical pathways could be found. In the present study, we investigated the locations of thethalamic neurons which receive inputs from thevestibular apparatus, particularly from the posterior semicircular canals, and further examined
the projections of the thalamic neurons to theASSS or PCD using anesthetized cats. We
hypothesized that the thalamic neurons receiving input from PC neurons could be located in
the ventrobasal complex and MGmc and could
contribute to the vestibulocortical pathways bymaking monosynaptic or polysynaptic connections with neurons in the ASSS or PCD.

Abbreviations: ASSS, anterior suprasylvian sulcus; MGmc, magnocellular nucleus of the medial geniculate
body; PC, posterior canal; PCD, postcruciate dimple

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Materials and Methods
Experiments were performed on 14 adult cats.
All procedures used in this study were reviewed
and fulfilled the requirements given in “Guidelines for animal experimentation” of the Facultyof Medicine, Tottori University and conformed

to standards set forth by the National Institute ofHealth’s “Guide for the care and use of animals.”
The animals were anesthetized with sodium
pentobarbital or alpha-chloralose (an initial
dose of 40 mg/kg, with a subsequent dose of 5mg/kg/h intraperitoneally). They were mounted in a stereotaxic apparatus which could besinusoidally rotated in pitch. Ag-AgCl elec-

A 7.0

CAUDAL
A 6.5

LPLG

CM

LPA 6.0

LG
MG

VPM

CMLG

MGPC
PCN

FRmc

MG

A 9.0
R
SN

A 8.0
MD
VL

LP

A 7.5
VPM
MD

VPL

LG

LP

MG
VPM

VPL

VPM

FFH

MM

ROSTRAL

VPL

FFH
2 mm

ASSS & PCD
PCD
ASSS

Fig. 1. Frontal plane projection of the brain stem showing distribution of 36 thalamic neurons. Drawings areof cross-sections of the mesodiencephalon on A 6.0, A 6.5, A 7.0, A 7.5, A 8.0 and A 9.0 Horsely-Clarke
planes. Each symbol indicates the sites where different projections of thalamic neurons were recorded. Theeffective sites for antidromic activation of thalamic neurons are indicated by symbols shown at the lower rightof the schema. ASSS, anterior suprasylvian sulcus; CG, central gray; CM, centromedian nucleus; FFH,Forel’s field H; FR, fasciculus retroflexus; LG, lateral geniculate nucleus; LP, lateral posterior nucleus; mc,magnocellular nucleus; MD, medial dorsal nucleus; MG, medial geniculate body; MM, medial mamillarynucleus; PC, posterior commissure; PCD, postcruciate dimple; PCN, posterior commissure nucleus; R, rednucleus; SN, substantia nigra; VL, ventral lateral nucleus; VPL, ventral posterolateral nucleus; VPM, ventral
posteromedial nucleus.

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Location of thalamo-cortical neurons

trodes were placed on the left round and oval
windows to stimulate the vestibular nerve(Shimazu and Precht, 1965). Then, 2 arrays of
8 concentric stimulating electrodes were positioned in the gray matter of the right PCD andthe ASSS to test projections of single thalamic
neurons to these regions. The electrode tips
were 1.0–1.5 mm deep from the cortical surface. Procedures for implantation were described in our previous paper (Matsuo et al., 1994,1995). Stimulus intensity was confined to lessthan 200 µA. A glass micropipette filled with 2mol/L NaCl solution, saturated with fast green
FCF, was employed for recording extracellularspikes of PC-activated thalamic neurons on theright side. Recorded extracellular spikes wereconsidered to originate from the soma if theyfulfilled the following criteria: i) the spike is biphasic negative-positive or predominantly negative with a clearly visible initial segment-soma
dendrite break and ii) the spike can be detectedsequentially in spite of any movement of therecording electrode over 100 µm. At the end ofeach experiment, the recording and stimulatingsites were histologically verified in Nisslstained serial sections of the brain for laterreconstruction (Thomas and Wilson, 1965).

Results
We examined the cell locations of PC-activatedthalamic neurons and their projections to theASSS and PCD. Thirty-six neurons were identified as posterior-canal activated thalamic
neurons when they were activated by the stimulation of the contralateral vestibular nerve andby nose-up head rotation in the dark. The identified neurons increased the firing frequency ofthe spikes during nose-up pitch rotation. Whenthe contralateral vestibular nerve was stimulated, the neurons were synaptically activated.
These latencies ranged from 2.1 to 11.5 ms.
Out of the 36 neurons, 8 neurons were antidromically activated only from the ASSS, 3
neurons from the PCD, and 2 neurons from both
the ASSS and PCD. The effective sites for
antidromic activation of the thalamic neurons
were mainly in the lateral part of the PCD andthe anterior part of the ASSS. The remaining 23
neurons did not induce any antidromic spikes
following stimulation of the ASSS and PCD.
Histological examination showed that mostof them were located in the ventral posterolateral and -medial nuclei and the lateral posterior nucleus. A smaller number of such neurons
were also found in the magnocellular nucleus of
the medial geniculate body (MGmc), as shownin Fig. 1.

Discussion
Cortical areas which receive input from the vestibular nerve are located in the PCD and ASSSin cats (Landgren et al., 1967; Sans et al., 1970;Ödkvist et al., 1975; Liedgren et al., 1976;
Mergner et al., 1981). These areas receive convergent inputs from proprioceptive, somatosensory and vestibular afferents via thalamic
neurons, and were thereby postulated to contribute to conscious spatial orientation (Sans etal., 1970; Schwarz and Fredrikson, 1971).
Thalamo-cortical neurons were studied byretrograde transport of horseradish peroxidase
injected into the PCD and ASSS in cats (Liedgrenet al., 1976; Blum et al., 1979; Mergner et al.,1981). The main location of these neurons arereported to be in the ventral posterolateral nucleus, posterior margin of the ventrobasal complex, and MGmc. Similarly, as we observed in
the present study, thalamic neurons which wereactivated by nose-up head rotation and bycontralateral vestibular nerve stimulation wererecorded mainly in the ventral posero-lateraland -medial nuclei, and some neurons werelocated in the MGmc, suggesting that the neurons in these areas receive input from the posterior semicircular canal. Thirteen of thesethalamic neurons were antidromically activatedfrom the ASSS and/or PCD of the cortex. Latencies of spikes of the identified thalamic
neurons followed by contralateral vestibular
nerve stimulation ranged from 2.1 ms to 11.5
ms. The shortest latencies of less than 2.9 ms
may be regarded as within the disynaptic range,
since latencies of monosynaptic activation ofvestibular nucleus neurons followed by ves-165

S. Matsuo et al.

tibular nerve stimulation are less than 1.4 ms(Uchino et al., 1982) and the latency of thenegative averaged potentials in the ventral posterolateral nucleus ranged from 0.8 ms to 1.5
ms, as shown in the previous studies (Matsuo etal., 1994,1995). Thus, the thalamic neurons
which were activated from the contralateral
vestibular nerve with the shortest latencies
probably received direct inputs from the PCrelated secondary vestibular nucleus neurons.
These results suggest that the thalamic neurons
projected to the ASSS and/or PCD in this study
contribute, at least in part, to the primary
vestibulo-cortical pathways.

Acknowledgments: This study was partly supported
by a Grant-in-Aid for Scientific Research (No.
07671848) from the Japanese Ministry of Education,
Science and Culture.
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(Received February 8, Accepted May 11, 1998)

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