Responses of locus coeruleus and subcoeruleus neurons to sinusoidal stimulation of labyrinth receptors

Abstract

In precollicular decerebrate cats the electrical activity of 141 individual neurons located in the locus coeruleus-complex, i.e. in the dorsal ( n = 41) and ventral parts ( n = 67) as well as in the locus subcoeruleus ( n = 33), was recorded during sinusoidal tilt about the longituclinal axis of the whole animal, leacling to stimulation of labyrinth receptors. Some of these neurons showed physiological characteristics attributed to the norepinephrine-containing locus coeruleus neurons, namely, (i) a slow and regular resting discharge, and (ii) a typical biphasic response to fore- and hindpaw compression consisting of short impulse bursts followed by a silent period, which has been attributed to recurrent and/or lateral inhibition of the norepinephrine-containing neurons. Furthermore, 16 out of the 141 neurons were activated antidromically by stimulation of the spinal cord at T 12 and L 1, thus being considered coeruleospinal or subcoeruleospinal neurons. A large number of tested neurons (80 out of 141, i.e. 56.7%) responded to animal rotation at the standard frequency of 0.15 Hz and at the peak amplitude of 10°. However, the proportion of responsive neurons was higher in the locus subcoeruleus (72.7%) and the dorsal locus coeruleus (61.0%) than in the ventral locus coeruleus (46.3%). A periodic modulation of firing rate of the units was observed during the sinusoidal stimulus. In particular, 45 out of the 80 units (i.e. 56.2%) were excited during side-up and depressed during side-down tilt (β-responses), whereas 20 of 80 units (i.e. 25.0%) showed the opposite behavior (α-responses). In both instances, the response peak occurred with an average phase lead of about +18°, with respect to the extreme side-up or side-down position of the animal; however, the response gain (imp./s per deg) was, on average, more than two-fold higher in the former than in the latter group. The remaining 15 units (i.e. 18.7%) showed a prominent phase shift of this response peak with respect to animal position. Similar results were obtained from the subpopulation of locus coeruleus-complex neurons which fired at a low rate (< 5.0 imp./s), as well as for the antidromically identified coeruleospinal neurons. The response gain of locus coeruleus-complex neurons, inclucling the coeruleospinal neurons, did not change when the peak amplitude of tilt was increased from 5° to 20° at the fixed frequency of 0.15 Hz. This indicates that the system was relatively linear with respect to the amplitude of displacement. When the frequency of stimulation was increased from 0.008 to 0.32 Hz at the fixed amplitude of 10°, the locus coeruleus-complex neurons showed either no change (static responses) or a slight increase in the response gain (dynamic responses). In several units the relative stability of the phase angle of the responses, evaluated with respect to the animal position, allowed for the attribution of these responses to both static or dynamic properties of the macular receptors. Some units, however, showed either an increase or a decrease in phase lead of responses when the frequency of tilt was increased; in the former instance the responses could be attributed to stimulation of the vertical canal receptors. These observations are discussed in relation to the fact that the locus coeruleus-complex exerts a direct inhibitory influence on Renshaw-cells. In particular, we postulate that periodic changes in firing rate of the antidromically identified coeruleospinal neurons during tilt might change the functional coupling of the ipsilateral limb extensor motoneurons with their own Renshaw-cells, thus intervening in the gain regulation of the corresponcling vestibulospinal reflex. As to the unidentified locus coeruleus-complex neurons responsive to tilt, they might be involved in the labyrinthine control of functions other than posture.