Parallel analyses of nociceptive neurones in rat superior colliculus by using c-fos immunohistochemistry and electrophysiology under different conditions of anaesthesia.

Multiple sensory inputs to the superior colliculus (SC) play an important role in guiding head and eye movements toward or away from biologically significant stimuli. Much is now known about the visual, auditory, and somatosensory response properties of SC neurones that mediate these behavioural reactions. Rather less is known about the responses of SC neurones to noxious stimuli, and thus far, most of this information has been obtained in anaesthetised animals. Therefore, the purpose of the present study was to use the c-fos immunohistochemical technique and standard extracellular electrophysiology as parallel measures of nociceptive activity in the SC under different conditions of anaesthesia. In unanaesthetised animals, experimental and control treatments induced a qualitatively similar pattern of Fos-like immunoreactivity (FLI) in the SC, which was quantitatively related to the severity or biologic salience of the treatment; thus, baseline control < control injections of saline < a nonpainful stressor (immobilisation) < noxious injections of formalin. Compared with baseline levels, urethane and avertin anaesthesia induced FLI expression in the SC intermediate layers, although the FLI response to both noxious stimulation and control conditions was differentially suppressed in different layers of the SC by anaesthesia. Parallel electrophysiologic recordings found that anaesthesia was associated with high levels of spontaneous activity in the SC intermediate layers, often in neurones which were also nociceptive. High rates of background spike activity were also induced in the SC intermediate layers by noxious stimulation in chronically recorded awake animals. Although these results point to some differences between the nociceptive responses of SC neurones in anaesthetised and unanaesthetised animals, both data sets support the view that there are different populations of nociceptive neurones in the rodent SC that may be related to different adaptive functions of pain.

Cerebellar output exerts spatially organized influence on neural responses in the rat superior colliculus.

The deep cerebellar nuclei project to largely segregated target regions in the contralateral superior colliculus. Single-unit recordings have previously shown that nuclear inactivation normally suppresses spontaneously active collicular target neurons. However, facilitation of activity has also been found in a proportion of collicular units. In the present study we tested the hypothesis that the type of effect is related to the cerebellotectal topography. We recorded simultaneously in the deep cerebellar nuclei and superior colliculus of 53 anaesthetized rats. GABA microinjections produced a complete, reversible, arrest of activity in the deep cerebellar nuclei. We investigated the effect of this inactivation on 292 sensory and non-sensory cells in the collicular intermediate and deep layers. Of these, 29% showed a reduced response to their preferred sensory stimulus or decreased their spontaneous firing rate in the case of non-sensory cells. However, 15% increased their sensory responsiveness and/or spontaneous firing rate following cerebellar inactivation. No effect was seen in the remaining 56% of cells. The distribution of these different effects was highly significantly related to the topography of the cerebellotectal terminal fields. Thus, 68% of the suppressive effects were obtained from cells lying in the terminal fields of the deep cerebellar nucleus inactivated. Conversely, 86% of the excitatory effects and 66% of the cells showing no effect were obtained from cells falling outside the terminal field. The results support the view that the superior colliculus is an important site for the functional integration of primary sensory information, not only with cortical and basal ganglia afferents, but also with cerebellar information. The contrasting physiological responses observed within the terminal cerebellotectal topography appear to map closely on to the known distribution of the cells of origin of the two major descending output pathways of the superior colliculus and are possibly mediated by intrinsic inhibitory connections within its intermediate and deep layers. These results provide evidence for a neural architecture in the superior colliculus whose function is the selection of appropriate actions in response to novel stimuli and the suppression of competing motor programmes.

Spatial variation in the effects of inactivation of substantia nigra on neuronal activity in rat superior colliculus.

Superior colliculus (SC)-mediated behaviours are under the disinhibitory control of the striato-nigro-collicular projection. We systematically investigated the homogeneity of substantia nigra pars reticulata (SNr) influence on different populations of SC neurons by recording the effects of intranigral GABA microinjections on 149 cells at different locations in the rat SC. Suppression of the tonic activity of SNr resulted in both the facilitation and paradoxical inhibition of spatially-segregated SC target neurons. These dual influences were found to broadly map onto the SC origins of the descending projections known to support approach and avoidance/defensive behaviours. These findings are consistent with an organisation which promotes contrasting processes for the selection of a behaviour and simultaneous suppression of competing motor programs.

Anticonvulsant and behavioural effects of bicuculline injected into the mesencephalic locomoter region of rats.

Previous microinjection mapping studies in the mesencephalon established a significant association between the induction of locomotor activation and the suppression of tonic seizures in the electroshock model of epilepsy. The purpose of the present study was to see if this relationship also applies in an area of the brainstem commonly known as the mesencephalic locomotor region (MLR). The principal findings were the following. (i) Activation of extensive areas of the dorsal midbrain and tegmentum, including the MLR, by unilateral injections of the GABA antagonist bicuculline induced leg movements and suppressed the tonic component of electroshock-induced seizures. (ii) A highly significant correlation was observed between these two variables. (iii) In some cases, however, the induction of phasic leg movements was neither sufficient nor necessary for tonic seizure suppression. It is possible, therefore, that injection-elicited changes in tonic aspects of limb control may be more directly related to the suppression of tonic motor seizures in the electroshock model of epilepsy.