Lateral geniculate spikes, muscle atonia and startle response elicited by auditory stimuli as a function of stimulus parameters and arousal state

Abstract

We have investigated the motor and ponto-geniculo-occipital (PGO) wave response to startle eliciting stimuli in the unanesthetized cat. We found that the amplitude of the PGO spike recorded in the lateral geniculate nucleus (LGN) increases monotonically with increasing intensities of auditory stimuli. In contrast, the motor response to low intensity (less than 75 dB) stimuli is characterized by electromyographic (EMG) suppression, while at higher intensities an EMG excitation is superimposed on this suppression. Thus PGO elicitation is accompanied by EMG suppression at low intensities and by a net EMG excitation at high intensities. While the amplitude of the auditory elicited PGO response is a graded function of stimulus intensity, somatic stimuli tend to elicit the PGO response in all-or-none fashion. Both the motor and PGO responses to sensory stimulation change with behavioral state. The EMG suppression by auditory stimulation increases in duration during the transition to rapid eye movement (REM) sleep. Elicited PGO amplitude is highest in transitional sleep, lower in quiet waking and REM sleep and lowest in active waking. Prepulse inhibition of PGO spikes is greatly attenuated during transitional and REM sleep. We hypothesize the existence of 3 phasic response systems, a motor suppression system, a motor excitation (startle) system and a PGO elicitation system. While these systems are triggered concurrently by intense phasic stimuli in waking, they are modulated independently by stimulus intensity and behavioral state, and have different rates of habituation. These systems act in concert to produce behavioral responses to sudden onset stimuli.

Fig. 1.

Oscilloscope traces of neck EMG and LGN spike response to a 105 dB, 20 ms noise burst. Five traces were superimposed. ST, stimulus as recorded through a microphone inside the recording cage.

Fig. 2.

Averaged EMG and LGN spike responses to click stimuli of varying intensities. Fifty trials were run at each intensity level. The vertical bars represent stimulus onset. The total duration of the trace was 200 ms.

Fig. 3.

Changes in the amplitude of LGN spikes evoked by a 115 dB click stimulus as a function of state. Data from 6 cats were averaged. Amplitudes were normalized as percentage of the largest amplitude of the spontaneous PGO waves during transition and REM for each cat.

Fig. 4.

Oscilloscope traces of LGN spikes elicited by a 115 dB click stimulus during non-REM (upper) and REM (lower) states. Eight traces were superimposed. The arrow indicates stimulus onset.

Fig. 5.

A: probability for eliciting LGN spike response with a 115 dB click, or a 1.5 mA somatic stimulus delivered through neck EMG electrode pairs, in different states. Data from 6 cats (auditory) and 2 cats (somatic) were averaged. B: effect of varying auditory stimulus intensity on probability of LGN spike elicitation in a single cat. In both figures data are expressed as percentage of trials with discrete responses.

Fig. 6.

Oscilloscope traces (left) and computer averaged (right) LGN and EMG responses to a 115 dB click (S) with and without a preceding 80 dB click prestimulus (P) in quiet waking. The interval between the prestimulus and the startle-eliciting stimulus was 100 msec. The total durations of the oscilloscope and computer-averaged traces were both 500 ms.

Fig. 7.

Effects of an auditory (70 dB click) and a somatic (0.7 mA electrical pulse) prestimulus on the amplitude of the LGN spike elicited by a subsequent auditory stimulus (115 dB click) in different states. Data are amplitude reduction (control minus prepulse) and expressed as the percentage of the control amplitude to the eliciting stimulus alone during the same state.

Fig. 8.

Oscilloscope traces of EMG and LGN spike response to an 105 dB click during periods of quiet waking (QW) and the transition from non-REM to REM (transition). The arrow indicates stimulus onset.

Fig. 9.

Startle amplitude to a 115 dB click with (prepulse) or without (control) a preceding 70 dB click stimulus during active waking (AW), quiet waking (QW) and non-REM sleep. Data are the average of 2 cats and normalized as the percentage of total response level across states.