Changes in the activity of units of the cat motor cortex with rapid conditioning and extinction of a compound eye blink movement

Abstract

Patterns of spike activity were measured in the pericruciate cortex of conscious cats before and after development of a Pavlovian conditioned eye blink response. Unit activity was tested with presentations of a click conditioned stimulus (CS) and a hiss discriminative stimulus (DS) of similar intensity to the click. Unit discharge in response to the CS increased after conditioning, but not after backward conditioning when conditioned reflexes (CRs) were not performed. Rates of spontaneous, baseline discharge were not increased after conditioning with respect to rates of discharge measured in the naive state. It appeared that an increase in the ratio of CS-elicited discharge to background activity, together with an increase in the number of units responding to the CS after conditioning, supported discrimination of the CS from the DS and performance of the conditioned blink response. This is the first detailed characterization of patterns of a rapidly conditioned Pavlovian response. Activation of units by the CS preceded the onset of the CR, supporting the hypothesis that the activity played a role in initiating the conditioned eye blink movement. Extinction with retention of performance of the CR was associated with perseverance of the increased unit discharge in response to the CS. Extinction with substantially reduced performance of the CR was associated with diminution of the unit response to the CS below levels found with conditioning. Averages of patterns of spike activity elicited by the CS after conditioning showed components of discharge with onsets of 8–40 msec (alpha 1), 40–72 msec (alpha 2), 72–112 msec (beta), and greater than 112 msec (gamma), corresponding to each of four separate excitatory EMG components of the compound blink CR. Each component increased in magnitude after conditioning, relative to levels found in the naive state. The finding that long- as well as short-latency components of unit activation increased after conditioning supported the hypothesis that generation of both long- and short-latency blink CRs in normal animals may depend significantly on neural circuitry and mechanisms within the motor cortex.

The Cerebellar Interpositus Nucleus and the Dynamic Control of Learned Motor Responses

“…These waves are present not only in the position, velocity, and acceleration profiles of eyelid traces (Domingo et al, 1997) but have also been noticed in the EMG activity of the orbicularis oculi muscle (Domingo et al, 1997), in the firing activity of facial motoneurons innervating this muscle (Trigo et al, 1999), in the resting potential of facial motoneurons recorded both in vivo (Trigo et al, 1999) and in vitro (Magarinos-Ascone et al, 1999), and, finally, in the firing activities of motor cortex neurons during CRs evoked in behaving cats (Aou et al, 1992).…”

Role of Cerebellar Interpositus Nucleus in the Genesis and Control of Reflex and Conditioned Eyelid Responses

“…Thus, muscimol injections damped the typical Ϸ20 Hz oscillation present in CRs, whereas microstimulation enhanced it. In fact, an oscillation of the same dominant frequency (Ϸ20 Hz) has been recorded in the EMG activity of the orbicularis oculi muscle (Domingo et al, 1997), in the membrane potential of rat facial motoneurons recorded in vitro (Magariños-Ascone et al, 1999), in the discharge rate of facial nucleus motoneurons recorded in alert behaving cats (Trigo et al, 1999), and in firing activities of motor cortex neurons during performance of CRs in cats (Aou et al, 1992). In contrast, our data do not support any role of interpositus nucleus in the initiation of acquired eyelid responses, but it might participate in their proper timing with respect to the US presentation (Koekkoek et al, 2003).…”

“…Furthermore, single and train stimuli applied to the PIN were unable to evoke reflex-like eyelid responses, indicating that this neural structure is unable per se to initiate noticeable blinks, unless in the presence of facilitative inputs arriving at orbicularis oculi motoneurons from trigeminal (for reflex) and cortical (for learned) origins (Aou et al, 1992;Trigo et al, 1999). The presence of extracerebellar components in learned eyelid responses has also been demonstrated recently in mutant mice in which the induction of long-term depression at the parallel fiberPurkinje cell synapse is impaired (Koekkoek et al, 2003).…”

Dynamic Associations in the Cerebellar–Motoneuron Network during Motor Learning

“…7B) acting before or after phase synchronization, respectively. The best candidate for this role is the cerebral motor cortex that participates in both the generation and dynamic control of learned movements (Aou et al, 1992;Troncoso et al, 2007). Thus, motoneuronal responses and cerebellar IP activities contain equal amounts of information about the common source.…”