SummaryOur tactile perception of external objects depends on skin-object interactions. The mechanics of contact dictates the existence of fundamental spatiotemporal input features—contact initiation and cessation, slip, and rolling contact—that originate from the fact that solid objects do not interpenetrate. However, it is unknown whether these features are represented within the brain. We used a novel haptic interface to deliver such inputs to the glabrous skin of finger/digit pads and recorded from neurons of the cuneate nucleus (the brain’s first level of tactile processing) in the cat. Surprisingly, despite having similar receptive fields and response properties, each cuneate neuron responded to a unique combination of these inputs. Hence, distinct haptic input features are encoded already at subcortical processing stages. This organization maps skin-object interactions into rich representations provided to higher cortical levels and may call for a re-evaluation of our current understanding of the brain’s somatosensory systems.

A common method to explore the somatosensory function of the brain is to relate skin stimuli to neurophysiological recordings. However, interaction with the skin involves complex mechanical effects. Variability in mechanically induced spike responses is likely to be due in part to mechanical variability of the transformation of stimuli into spiking patterns in the primary sensors located in the skin. This source of variability greatly hampers detailed investigations of the response of the brain to different types of mechanical stimuli. A novel stimulation technique designed to minimize the uncertainty in the strain distributions induced in the skin was applied to evoke responses in single neurons in the cat. We show that exposure to specific spatio-temporal stimuli induced highly reproducible spike responses in the cells of the cuneate nucleus, which represents the first stage of integration of peripheral inputs to the brain. Using precisely controlled spatio-temporal stimuli, we also show that cuneate neurons, as a whole, were selectively sensitive to the spatial and to the temporal aspects of the stimuli. We conclude that the present skin stimulation technique based on localized differential tractions greatly reduces response variability that is exogenous to the information processing of the brain and hence paves the way for substantially more detailed investigations of the brain's somatosensory system.

To any model of brain function, the variability of neuronal spike firing is a problem that needs to be taken into account. Whereas the synaptic integration can be described in terms of the original Hodgkin-Huxley (H-H) formulations of conductance-based electrical signaling, the transformation of the resulting membrane potential into patterns of spike output is subjected to stochasticity that may not be captured with standard single neuron H-H models. The dynamics of the spike output is dependent on the normal background synaptic noise present in vivo, but the neuronal spike firing variability in vivo is not well studied. In the present study, we made long-term whole cell patch clamp recordings of stationary spike firing states across a range of membrane potentials from a variety of subcortical neurons in the non-anesthetized, decerebrated state in vivo. Based on the data, we formulated a simple, phenomenological model of the properties of the spike generation in each neuron that accurately captured the stationary spike firing statistics across all membrane potentials. The model consists of a parametric relationship between the mean and standard deviation of the inter-spike intervals, where the parameter is linearly related to the injected current over the membrane. This enabled it to generate accurate approximations of spike firing also under inhomogeneous conditions with input that varies over time. The parameters describing the spike firing statistics for different neuron types overlapped extensively, suggesting that the spike generation had similar properties across neurons.

In the present paper we apply a new neurophysiological technique to make single-electrode, dual loose-patch recordings from pairs of neuronal elements in the cerebellar cortex in vivo. The analyzed cell pairs consisted of an inhibitory molecular layer interneuron and a Purkinje cell (PC) or a Golgi cell and a granule cell, respectively. To detect the magnitude of the unitary inhibitory synaptic inputs we used histograms of the spike activity of the target cell, triggered by the spikes of the inhibitory cell. Using this analysis, we found that single interneurons had no detectable effect on PC firing, which could be explained by an expected very low synaptic weight of individual interneuron-PC connections. However, interneurons did have a weak delaying effect on the overall series of interspike intervals of PCs. Due to the very high number of inhibitory synapses on each PC, a concerted activation of the interneurons could still achieve potent PC inhibition as previously shown. In contrast, in the histograms of the Golgi cell-granule cell pairs, we found a weak inhibitory effect on the granule cell but only at the time period defined as the temporal domain of the slow IPSP previously described for this connection. Surprisingly, the average granule cell firing frequency sampled at one second was strongly modulated with a negative correlation to the overall firing level of the Golgi cell when the latter was modified through current injection via the patch pipette. These findings are compatible with that tonic inhibition is the dominant form of Golgi cell-granule cell inhibition in the adult cerebellum in vivo.

Spinocerebellar systems are likely to be crucial for cerebellar hallmark functions such as coordination. However, in terms of cerebellar functional analyses, these are perhaps among the least explored systems. The aim of the present study is to achieve activation of a single component of the spinocerebellar systems and to explore to what extent it can influence the spike output of granule cells, Golgi cells, molecular layer (ML) interneurons (stellate and basket cells) and Purkinje cells (PCs). For this purpose, we took advantage of a unique arrangement discovered in neuroanatomical studies, in which the spinal border cell (SBC) component of the ventral spinocerebellar system was found to be the only spinocerebellar tract which ascends in the contralateral lateral funiculus (coLF) and have terminations in sublobulus C1 of the paramedian lobule in the posterior cerebellum. Using electrical stimulation of this tract, we find a subset of the cerebellar cortical neurons in this region to be moderately or powerfully activated. For example, some of our granule cells displayed high intensity responses whereas the majority of the granule cells displayed no response at all. The finding that more than half of the PCs were activated by stimulation of the SBC tract indicated that this system is capable of directly influencing cerebellar cortical output. The implications of these findings for the view of the integrative functions of the cerebellar cortex are discussed.