In Vivo Responsiveness of LC Neurons 1 Spontaneous Activity

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The spontaneous discharge of LC neurons varies with the stage of sleep-wake cycle, 2 Hz during waking, lower during slow-wave sleep (from ~ 1.5 Hz in stage 2 to ~0.2 Hz in stage 4), and virtually absent during paradoxical sleep (~0.02 Hz). Rate of discharge also varies during different kinds of waking behavior, suggesting that LC activity is correlated with the state of arousal even during waking. Typically, LC neurons exhibit relatively little activity during low-vigilance behavior, such as grooming and food consumption, whereas their activity increases during exploratory behavior.

2. Responsiveness to Sensory Stimuli

LC neurons also exhibit phasic responses of short latencies (15-50 msec) to sensory stimuli in every modality (auditory, visual, somatosensory, and olfactory). These responses consist of a brief excitation followed by an inhibition lasting for several hundred milliseconds.

The responsiveness of LC varies between species. In rats, any of a variety of intense stimuli evokes LC responses in a majority of sensory trials. However, the response habituates with repetitive stimulus presentation. In monkeys, LC is influenced less strongly by intense stimuli, but again, when responses occur, they fade after the first few trials. Intense conspicuous stimuli that interrupt behavior and elicit an orientating response reliably induce a LC response. Similarly, in complex behavioral tasks such as the oddball, where target cues are presented in a semirandom fashion with nontarget cues, target stimuli, even nonintense, are sufficient to induce a LC response (Fig. 5).

In cats, when the animal is well-habituated to its environment and is in a quiet waking state, LC neurons often display very little response to previously presented neutral stimuli. The presentation of novel or noxious stimuli will, in contrast, elicit a burst of unit activity (see the following section).

More generally, it can be considered that tonic activity of noradrenergic LC neurons is highly correlated with changing degree of alertness, whereas LC neurons respond phasically to behaviorally significant stimuli.

3. Responsiveness to Stressful Stimuli

Stressful stimuli such as confrontation with a dog (for cats), footshock, cold environment, loud noise, and immobilization reliably stimulate LC activity, an excitation usually accompanied by a sympathetic activation. This has led to the proposal of the LC as a central analog of peripheral sympathetic ganglia.

Physiological stress (hypotensive challenge, bladder distension, colon distension, and sciatic nerve stimulation) also reliably stimulates LC neurons even in nonnoxious magnitudes. Some of these effects are mediated via CRF release within the LC (for example, hypotensive stress as previously mentioned), but this is not the rule and different stresses act through different mechanisms.

Whereas chronic presentation of a nonnoxious stimulus results in the diminution of the LC response, chronic stress often results in sensitized noradrenergic activation by a subsequent stress. This noradrenergic

Figure 5 Noradrenergic neuron responses during the odd ball task. In the odd ball task, either vertical or horizontal bars are presented to monkeys. The activity of their noradrenergic neurons is shown here in a peristimulus histogram, which means that all recorded responses were added, with time zero corresponding to stimulus presentation (arrows). In A, vertical bars are presented in 10% of the trials and the animal response is rewarded ( + ). Horizontal bars are presented in 90% of the trials and are not rewarded (—). In B, the rule is reversed. Horizontal bars are presented 10% of the time and rewarded ( + ), whereas vertical bars are presented 90% of the time and not rewarded (—). In C, the initial rule is back. LC neuron firing is specifically increased by the presentation of the rewarding stimulus. From Aston-Jones, G., et al. (1999). Attention. In Fundamental Neuroscience, Academic Press, San Diego.

Figure 5 Noradrenergic neuron responses during the odd ball task. In the odd ball task, either vertical or horizontal bars are presented to monkeys. The activity of their noradrenergic neurons is shown here in a peristimulus histogram, which means that all recorded responses were added, with time zero corresponding to stimulus presentation (arrows). In A, vertical bars are presented in 10% of the trials and the animal response is rewarded ( + ). Horizontal bars are presented in 90% of the trials and are not rewarded (—). In B, the rule is reversed. Horizontal bars are presented 10% of the time and rewarded ( + ), whereas vertical bars are presented 90% of the time and not rewarded (—). In C, the initial rule is back. LC neuron firing is specifically increased by the presentation of the rewarding stimulus. From Aston-Jones, G., et al. (1999). Attention. In Fundamental Neuroscience, Academic Press, San Diego.

sensitization parallels an increased behavioral response.

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