THE BRAIN-STEM PARABRACHIAL REGION CONTROLS MODE OF RESPONSE TO VISUAL-STIMULATION OF NEURONS IN THE CATS LATERAL GENICULATE-NUCLEUS

We recorded the responses of neurons from the cat's lateral geniculate nucleus to drifting sine-wave grating stimuli both before and during electrical stimulation of the parabrachial region of the midbrain. The parabrachial region provides a mostly cholinergic input to the latera l geniculate nucleus, and our goal was to study its effect on response s of geniculate cells to visual stimulation. Geniculate neurons respon d to visual stimuli in one of two modes. At relatively hyperpolarized membrane potentials, low threshold (LT) Ca2+ spikes are activated, lea ding to high-frequency burst discharges (burst mode). At more depolari zed levels, the low threshold Ca2+ spike is inactivated, permitting a more tonic response (relay or tonic mode). During our intracellular re cordings of geniculate cells, we found that, at initially hyperpolariz ed membrane potentials, LT spiking in response to visual stimulation w as pronounced, but that parabrachial activation abolished this LT spik ing and associated burst discharges. Coupled with the elimination of L T spiking, parabrachial activation also led to a progressive increase in tonic responsiveness. Parabrachial activation thus effectively swit ched the responses to visual stimulation of geniculate neurons from th e burst to relay mode. Accompanying this switch was a gradual depolari zation of resting membrane potential by about 5-10 mV and a reduction in the hyperpolarization that normally occurs in response to the inhib itory phase of the visual stimulus. Presumably, the membrane depolariz ation was sufficient to inactivate the LT spikes. We were able to exte nd and confirm our intracellular observations on the effects of parabr achial activation to a sample of cells recorded extracellularly. This was made possible by adopting empirically determined criteria to disti nguish LT bursts from tonic responses solely on the basis of the tempo ral pattern of action potentials. During parabrachial activation, ever y cell responded only in the relay mode, an effect that corresponds to our intracellular observations. We quantified the effects of parabrac hial activation on various response measures. The fundamental Fourier response amplitude (F1) was calculated separately for the total respon se, the tonic response component, and the LT burst component. Parabrac hial activation resulted in an increased F1 amplitude for the total re sponse. This increase was due to an increase in the tonic response com ponent. For a subset of cells showing epochs of LT bursting, parabrach ial activation concurrently reduced LT bursting and increased the ampl itude of the tonic response. Parabrachial activation, by eliminating L T bursting, also caused cells to respond with more linearity. By keepi ng geniculate cells in the relay mode, the parabrachial region serves to maintain a more linear retinogeniculate transfer of information to cortex, and this may be important for detailed analysis of visual targ ets. However, when a geniculate neuron becomes hyperpolarized, as may occur during states of visual inattention, it would not respond well t o visual stimuli without the sort of nonlinear amplification provided by the LT spike. Thus, the LT spike may permit hyperpolarized cells to relay to cortex the presence of a potentially salient or dangerous st imulus, but this is done at the expense of linearity, This may serve a s a sort of ''wake-up call'' that redirects attention to a particular stimulus and eventually enhances activity of appropriate parabrachial inputs to switch the critical geniculate neurons into the relay mode.