Functional properties of brainstem motoneurons following their reinnervation of native or foreign muscles.
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Animals↗
Biomedical subjects
A Gruart
Publications and source records attributed to A Gruart.
Firing activities of identified posterior interpositus nucleus neurons during associative learning in behaving cats.
On the basis of stimulation and permanent or transient lesions of putatively involved structures, and using transgenic mice with defective functional circuits, it has been proposed that cerebellar cortex and/or nuclei could be the sites where classically conditioned nictitating membrane/eyelid responses are acquired and stored. Here, we review recent information regarding the electrical activities of deep cerebellar nuclei neurons recorded during the performance of reflex and acquired eyeblinks. In particular, the rostral pole of the dorsolateral region of the posterior interpositus nucleus contains neurons significantly related to reflexively evoked and classically conditioned eyelid responses. Thus, type A interpositus neurons increase their discharge rate during eyelid movements, modulating it depending upon eyelid motorics. In contrast, type B neurons decrease their firing, even to a stop, during the same eyelid responses. However, as these changes in firing start after the onset of eyelid conditioned responses (CRs), and because they do not seem to encode eyelid position and velocity during the CR, the interpositus nucleus cannot be conclusively considered the site where eyelid learned responses are generated and stored. Additional microstimulation and pharmacological blockage of the recorded sites support the suggestion that posterior interpositus neurons contribute to the enhancement of CRs. Moreover, interpositus neurons probably contribute to the proper damping of newly acquired eyelid responses. The contributing role of other neuronal centers and circuits related to the eyelid motor system are also discussed.
Action Potentials↗
Motoneuron adaptability to new motor tasks following two types of facial-facial anastomosis in cats.
The ability of the facial motor system to adapt to a new motor function was studied in alert cats after unilateral transection, 180 degrees rotation and suture of the zygomatic nerve, or transection and cross-anastomosis of the proximal stump of the buccal nerve to the distal stump of the zygomatic nerve. These procedures induced reinnervation of the orbicularis oculi (OO) muscle by different OO- or mouth-related facial motoneurons. Eyelid movements and the electromyographic activity of the OO muscle were recorded up to 1 year following the two types of anastomosis. Animals with a zygomatic nerve rotation recovered spontaneous and reflex responses, but with evident deficits in eyelid kinematics, i.e. the proper regional distribution of OO motor units was disorganized by zygomatic nerve rotation and resuture, producing a permanent defect in eyelid motor performance. Following buccal-zygomatic anastomosis, the electrical activity of the OO muscle was recovered after 6-7 weeks, but air puff-, flash- and tone-evoked reflex blinks never reached the control values on the operated side. Electromyographic OO activities and lid movements corresponding to licking and deglutition activities were observed on the operated side in buccal-zygomatic anastomosed animals up to 1 year following surgery. Mouth-related facial motoneurons did not readapt their discharges to the kinetic, timing and oscillatory properties of OO muscle fibres. A significant hyper-reflexia was observed following both types of nerve repair in response to air puffs, but not to light flashes or tones. In conclusion, adult mammal facial premotor circuits maintain their motor programmes when motoneurons are induced to reinnervate a foreign muscle, or even a new set of muscle fibres.
Adaptation, Physiological↗
The role of interpositus nucleus in eyelid conditioned responses.
One of the most widely used experimental models for the study of learning processes in mammals has been the classical conditioning of nictitating membrane/eyelid responses, using both trace and delay paradigms. Mainly on the basis of permanent or transitory lesions of putatively-involved structures, and using other stimulation and recording techniques, it has been proposed that cerebellar cortex and/or nuclei could be the place/s where this elemental form of associative learning is acquired and stored. We have used here an output-to-input approach to review recent evidence regarding the involvement of the cerebellar interpositus nucleus in the acquisition of these conditioned responses (CRs). Eyelid CRs appear to be different in profile, duration, and peak velocity from reflexively-evoked blinks. In addition, CRs are generated in a quantum manner across conditioning sessions, suggesting a gradual neural process for their proper acquisition. Accessory abducens and orbicularis oculi motoneurons have different membrane properties and contribute differently to the generation of CRs, with significant species differences. In particular, facial motoneurons seem to encode eyelid velocity during reflexively-evoked blinks and eyelid position during CRs, two facts suggestive of a differential somatic versus dendritic arrival of specific motor commands for each type of movement. Identified interpositus neurons recorded in alert cats during classical conditioning of eyelid responses show firing properties suggestive of an enhancing role for CR performance. However, as their firing started after CR onset, and because they do not seem to encode eyelid position during the CR, the interpositus nucleus cannot be conclusively considered as the place where this acquired motor response is generated. More information is needed regarding neural signal transformations taking place in each involved neural center, and it its proposed that more attention should be paid to functional states (as opposed to neural sites) able to generate motor learning in mammals. The contribution of feedforward mechanisms normally involved in the processing activities of related centers and circuits, and the possible functional interactions within neural systems subserving the associative strength between the conditioned and unconditioned stimuli, are also considered.
Action Potentials↗
Hypoglossal and reticular interneurons involved in oro-facial coordination in the rat.
Chewing, swallowing, breathing, and vocalization in mammals require precise coordination of tongue movements with concomitant activities of the mimetic muscles. The neuroanatomic basis for this oro-facial coordination is not yet fully understood. After the stereotaxic microinjection of retrograde and anterograde neuronal tracers (biotin-dextran, Fluoro-Ruby, Fluoro-Emerald, and Fluoro-Gold) into the facial and hypoglossal nuclei of the rat, we report here a direct bilateral projection of hypoglossal internuclear interneurons onto facial motoneurons. We also confirm the existence of a small pool of neurons in the dorsal part of the brainstem reticular formation that project ipsilaterally to both facial and hypoglossal nuclei. For precise tracer injections, both motor nuclei were located and identified by the electrical antidromic activation of their constituent motoneurons. Injections of retrograde tracers into the facial nucleus consistently labeled neurons in the hypoglossal nucleus. These neurons prevalently lay in the ipsilateral side, were small in size, and, like classic intrinsic hypoglossal local-circuit interneurons, had several thin dendrites. Reverse experiments - injections of anterograde tracers into the hypoglossal nucleus - labeled fine varicose nerve fiber terminals in the facial nucleus. These fiber terminals were concentrated in the intermediate subdivision of the facial nucleus, with a strong ipsilateral prevalence. Double injections of different tracers into the facial and the hypoglossal nuclei revealed a small, but constant, number of double-labeled neurons located predominantly ipsilateral in the caudal brainstem reticular formation. Hypoglossal internuclear interneurons projecting to the facial nucleus, as well as those neurons of the parvocellular reticular formation that project to both facial and hypoglossal nuclei, could be involved in oro-facial coordination.
Animals↗
Harmaline induces different motor effects on facial vs. skeletal-motor systems in alert cats.
Harmaline's effects on reflex and classically conditioned eyelid responses and on tremor picked up by a coil attached to the back were measured in alert cats. Harmaline at a dose of 10 mg/kg produced skeletal muscle tremogenic effects that lasted 4h. Back movements presented a tremor-like displacement with a frequency peak at 10 Hz, but lid responses oscillated as in controls, at 20 Hz during both reflex and conditioned eyelid movements, with no increase in oscillation amplitude or frequency. The learning curves of harmaline-injected animals remained as in controls, but eyelid conditioned responses showed longer latencies, and smaller amplitude and peak velocity. Reflex and already-learned eyelid responses were not modified by harmaline. These results imply that neuronal control systems for skeletal-motor and facial responses are differentially affected by harmaline.
Journal Article↗
Hippocampal pyramidal cell activity encodes conditioned stimulus predictive value during classical conditioning in alert cats.
We have recorded the firing activities of hippocampal pyramidal cells throughout the classical conditioning of eyelid responses in alert cats. Pyramidal cells (n = 220) were identified by their antidromic activation from the ipsilateral fornix and according to their spike properties. Upper eyelid movements were recorded with the search coil in a magnetic field technique. Latencies and firing profiles of recorded pyramidal cells following the paired presentation of conditioned (CS) and unconditioned (US) stimuli were similar, regardless of the different sensory modalities used as CS (tones, air puffs), the different conditioning paradigms (trace, delay), or the different latency and topography of the evoked eyelid conditioned responses. However, for the three paradigms used here, evoked neuronal firing to CS presentation increased across conditioning, but remained unchanged for US presentation. Contrarily, pyramidal cell firing was not modified when the same stimuli used here as CS and US were presented unpaired, during pseudoconditioning sessions. Pyramidal cell firing did not seem to encode eyelid position, velocity, or acceleration for either reflex or conditioned eyelid responses. Evoked pyramidal cell responses were always in coincidence with a beta oscillatory activity in hippocampal extracellular field potentials. In this regard, the beta rhythm represents a facilitation, or permissive time window, for timed pyramidal cell firing. It is concluded that pyramidal cells encode CS-US associative strength or CS predictive value.
Acoustic Stimulation↗
Scopolamine impairs information processing in the hippocampus and performance of a learned eyeblink response in alert cats.
The object of this work was to determine whether the changes in field activity and neuronal excitability recorded in the hippocampus during eyeblink classical conditioning are induced by the cholinergic input, and their relationships with the conditioned response performance. The pyramidal layer field activity, its response to fornix stimulation and eyelid responses were recorded during paired tone-air puff presentations, under scopolamine (25, 50 and 100 microg/kg) or saline administration, following well-established eyeblink conditioning in a trace paradigm in cats. Scopolamine impaired behavioral performance, and, in the hippocampus, disrupted conditioned stimulus-evoked field potential, high frequency shift in field activity, and paired presentation-induced hyperexcitability. These findings indicate that the cholinergic input participates in hippocampal information processing in a way that allows precise conditioned response performance and memory trace formation.
Animals↗
[Morphological connections between the Hypoglassal and facial nerve in the brain stem of the rat].
BACKGROUND AND OBJECTIVE: The perfect coordination and synchronization of hypoglossal and facial muscles during chewing, swallowing, breathing, and vocalization requires particular concomitant activities of the facial muscles. In contrast, no direct connection between the facial and hypoglossal nucleus on the level of the brain stem has been detected until now. PATIENTS/METHODS: Facial and hypoglossal nuclei of rats were identified on the basis of their antidromic field potential recorded after peripheral stimulation of the corresponding nerves. Stereotactically single or double fluorescence tracer injections (Biotin-Dextran, Fluorescine-Dextran, Rhodamine-Dextran, Fluoro Gold) were placed into the nuclei. RESULTS: Retrograde tracer injections into the facial nucleus consistently labeled small neurons in the hypoglossal nucleus. In reverse experiments the injection of anterograde tracers into the hypoglossal nucleus labeled fine caliber varicose nerve fibers, but no somata in the facial nucleus. Synchronous injections of different tracers into the facial and hypoglossal nucleus produced a small, but constant number of double-labeled cells in the parvocellular reticular formation. CONCLUSIONS: Both, hypoglossal interneurons projecting to the facial nucleus and neurons of the parvocellular reticular formation double-projecting to the facial and hypoglossal nucleus might play an important role in coordinated orofacial movements. Moreover, both populations of neurons might be responsible for the excellent postoperative results after hypoglossal-facial anastomosis.
Animals↗
Involvement of cerebral cortical structures in the classical conditioning of eyelid responses in rabbits.
The classical conditioning of the eyelid motor system in alert behaving rabbits has been used to study the expression of Fos in the hippocampus, and in the occipital, parietal, piriform and temporal cortices. Animals were classically conditioned with both delay and trace conditioning paradigms. As conditioned stimulus, both short and long (20 and 100 ms) tones (600 Hz, 90 dB) or short, weak (20 ms, 1kg/cm(2)) air puffs were used. The unconditioned stimulus was always a long, strong (100 ms, 3 kg/cm(2)) air puff that started 250-270 ms after the onset of the conditioned stimulus. The expression of Fos was significantly increased after both delayed and trace conditioning in the hippocampus, and in the parietal and piriform cortices contralateral to the unconditioned stimulus presentation side, compared with equivalent ipsilateral structures in conditioned animals, or with Fos production in the same contralateral structures in pseudo-conditioned and control animals. Fos expression in some cortical sites was specific to tone versus air puff stimuli when used as conditioned stimulus. Thus, Fos expression was significantly increased in the contralateral temporal lobe when tones were used as conditioned stimulus, for both delayed and trace conditioning paradigms, but not when animals were conditioned to short, weak air puffs. The present results indicate a specific Fos activation in several cerebral cortical structures during associative eyelid conditioning.
Animals↗
Kinetic and frequency-domain properties of reflex and conditioned eyelid responses in the rabbit.
Eyelid position and the electromyographic activity of the orbicularis oculi muscle were recorded unilaterally in rabbits during reflex and conditioned blinks. Air-puff-evoked blinks consisted of a fast downward phase followed sometimes by successive downward sags. The reopening phase had a much longer duration and slower peak velocity. Onset latency, maximum amplitude, peak velocity, and rise time of reflex blinks depended on the intensity and duration of the air puff-evoking stimulus. A flashlight focused on the eye also evoked reflex blinks, but not flashes of light, or tones. Both delayed and trace classical conditioning paradigms were used. For delayed conditioning, animals were presented with a 350-ms, 90-dB, 600-Hz tone, as conditioned stimulus (CS). For trace conditioning, animals were presented with a 10-ms, 1-k/cm(2) air puff, as CS. The unconditioned stimulus (US) consisted of a 100-ms, 3-k/cm(2) air puff. The stimulus interval between CS and US onsets was 250 ms. Conditioned responses (CRs) to tones were composed of downward sags that increased in number through the successive conditioning sessions. The onset latency of the CR decreased across conditioning at the same time as its maximum amplitude and its peak velocity increased, but the time-to-peak of the CR remained unaltered. The topography of CRs evoked by short, weak air puffs as the CS showed three different components: the alpha response to the CS, the CR, and the reflex response to the US. Through conditioning, CRs showed a decrease in onset latency, and an increase in maximum amplitude and peak velocity. The time-to-peak of the CR remained unchanged. A power spectrum analysis of reflex and conditioned blink acceleration profiles showed a significant approximately 8-Hz oscillation within a broadband of frequencies between 4 and 15 Hz. Nose and mandible movements presented power spectrum profiles different from those characterizing reflex and conditioned blinks. It is concluded that eyelid reflex responses in the rabbit present significant differences from CRs in their profiles and metric properties, suggesting different neural origins, but that a common approximately 8-Hz neural oscillator underlies lid motor performance. According to available data, the frequency of this putative oscillator seems to be related to the species size.
Air Movements↗
Cerebellar posterior interpositus nucleus as an enhancer of classically conditioned eyelid responses in alert cats.
Cerebellar posterior interpositus neurons were recorded in cats during delayed and trace conditioning of eyeblinks. Type A neurons increased their firing in the time interval between conditioned and unconditioned stimulus presentations for both paradigms, while type B neurons decreased it. The discharge of different type A neurons recorded across successive conditioning sessions increased, with slopes of 0.061-0.078 spikes/s/trial. Both types of neurons modified their firing several trials in advance of the appearance of eyelid conditioned responses, but for each conditioned stimulus presentation their response started after conditioned response onset. Interpositus microstimulation evoked eyelid responses similar in amplitude and profiles to conditioned responses, and microinjection of muscimol decreased conditioned response amplitude. It is proposed that the interpositus nucleus is an enhancer, but not the initiator, of eyelid conditioned responses.
Action Potentials↗
Role of proprioception in the control of lid position during reflex and conditioned blink responses in the alert behaving cat.
The contribution of the orbicularis oculi muscle to the determination of lid position, and the putative role of eyelid proprioception in the control of reflex and conditioned eye blinks, were studied in alert behaving cats. Upper lid movements and the electromyographic activity of the orbicularis oculi muscle were recorded during reflexively evoked blinks and during the classical conditioning of the eyelid response. Blinks were evoked by air puffs, flashes and electrical stimulation of the supraorbitary branch of the trigeminal nerve. Eyelid responses were conditioned with a trace classical conditioning paradigm consisting of a short, weak air puff, followed 250 ms later by a long, strong air puff. Orbicularis oculi muscle activation during reflex blinks was independent of lid position and was not modified by the presence of weights acting in the upward or downward directions. Local anesthesia of the supraorbital nerve reduced blinks evoked by air puffs applied to the lower jaw, but did not affect flash-evoked blinks. No relationship was established between initial lid position and the first downward component of conditioned eyelid responses. In contrast, initial lid position was related to the first upward component of the same conditioned response. It is concluded that orbicularis oculi motor units receive no feedback proprioceptive signals from the eyelid, other than those coming from cutaneous receptors, and that lid position is determined by the activity of the levator palpebrae superioris muscle. The lack of sensory information about lid position in facial motoneurons probably has some functional implications on the central control of cognitive and emotional facial expressions.
Air↗
Discharge profiles of abducens, accessory abducens, and orbicularis oculi motoneurons during reflex and conditioned blinks in alert cats.
The discharge profiles of identified abducens, accessory abducens, and orbicularis oculi motoneurons have been recorded extra- and intracellularly in alert behaving cats during spontaneous, reflexively evoked, and classically conditioned eyelid responses. The movement of the upper lid and the electromyographic activity of the orbicularis oculi muscle also were recorded. Animals were conditioned by short, weak air puffs or 350-ms tones as conditioned stimuli (CS) and long, strong air puffs as unconditioned stimulus (US) using both trace and delayed conditioning paradigms. Motoneurons were identified by antidromic activation from their respective cranial nerves. Orbicularis oculi and accessory abducens motoneurons fired an early, double burst of action potentials (at 4-6 and 10-16 ms) in response to air puffs or to the electrical stimulation of the supraorbital nerve. Orbicularis oculi, but not accessory abducens, motoneurons fired in response to flash and tone presentations. Only 10-15% of recorded abducens motoneurons fired a late, weak burst after air puff, supraorbital nerve, and flash stimulations. Spontaneous fasciculations of the orbicularis oculi muscle and the activity of single orbicularis oculi motoneurons that generated them also were recorded. The activation of orbicularis oculi motoneurons during the acquisition of classically conditioned eyelid responses happened in a gradual, sequential manner. Initially, some putative excitatory synaptic potentials were observed in the time window corresponding to the CS-US interval; by the second to the fourth conditioning session, some isolated action potentials appeared that increased in number until some small movements were noticed in eyelid position traces. No accessory abducens motoneuron fired and no abducens motoneuron modified their discharge rate for conditioned eyelid responses. The firing of orbicularis oculi motoneurons was related linearly to lid velocity during reflex blinks but to lid position during conditioned responses, a fact indicating the different neural origin and coding of both types of motor commands. The power spectra of both reflex and conditioned lid responses showed a dominant peak at approximately 20 Hz. The wavy appearance of both reflex and conditioned eyelid responses was clearly the result of the high phasic activity of orbicularis oculi motor units. Orbicularis oculi motoneuron membrane potentials oscillated at approximately 20 Hz after supraorbital nerve stimulation and during other reflex and conditioned eyelid movements. The oscillation seemed to be the result of both intrinsic (spike afterhyperpolarization lasting approximately 50 ms, and late depolarizations) and extrinsic properties of the motoneuronal pool and of the circuits involved in eye blinks.
Abducens Nerve↗
Involvement of cerebellar cortex and nuclei in the genesis and control of unconditioned and conditioned eyelid motor responses.
The eyelid motor system of the cat was used here for the study of the kinetic properties of reflex and conditioned lid movements, and of the role played by the cerebellum in the acquisition and/or performance of both types of motor responses. Spontaneous blinks, eyelid reflex responses, eye-guided lid movements and conditioned lid responses were recorded in alert cats in simultaneity with unitary and field electrical activity of cerebellar cortex and nuclear zones related to the eyelid motor system. Results indicate that nuclear unitary activity does not precede unconditioned or conditioned lid responses, but that cerebellar nuclei are directly involved in the performance of the late components of reflex lid movements and in the acquisition of conditioned lid responses.
Action Potentials↗
Quantal organization of reflex and conditioned eyelid responses.
Quantal organization of reflex and conditioned eyelid responses. J. Neurophysiol. 78: 2518-2530, 1997. Upper lid movements and the electromyographic activity of the orbicularis oculi muscle were recorded in behaving cats during spontaneous and experimentally evoked reflex blinks, and conditioned eyelid responses. Reflex blinks evoked by the presentation of air puffs, flashes, or tones consisted of a fast downward lid movement followed by late, small downward waves, recurring at approximately 50-ms intervals. The latency, maximum amplitude, peak velocity, and number of late waves depended on the modality, intensity, and duration of the evoking stimulus. The power spectra of acceleration records indicated a dominant frequency of approximately 20 Hz for air puff-evoked blinks. Flashes and tones usually evoked small and easily fatigable reflex responses of lower dominant frequencies (14-17 and 9-11 Hz, respectively). A basic approximately 20-Hz oscillation was also noticed during lid fixation, and ramplike lid displacements evoked by optokinetic stimuli. Five classical conditioning paradigms were used to analyze the frequency-domain properties of conditioned eyelid responses. These learned lid movements differed in latency, maximum amplitude, and profile smoothness depending on the modality (air puff, tone), intensity (weak, strong), and presentation site (ipsi-, contralateral to the unconditioned stimulus) of the conditioned stimulus. It was found that the characteristic ramplike profile of a conditioned response was not smooth, but appeared to be formed by a succession of small waves at a dominant frequency of approximately 20 Hz. The amplitude (and number) of the constituting waves depended on the characteristics of the conditioned stimulus and on the time interval until unconditioned stimulus presentation. Thus conditioned responses seemed to be formed from lid displacements of 2-6 degrees in amplitude and approximately 50 ms in duration, which increased in number throughout conditioning sessions, until a complete (i.e., lid closing) conditioned response was reached. It is suggested that a approximately 20-Hz oscillator underlies the generation of reflex and conditioned eyelid responses. The oscillator is susceptible to being neurally modulated to modify the velocity of a given quantum of movement, and the total duration of the lid response. Learned eyelid movements are probably the result of a successively longer release of the oscillator as a function of the temporal-spatial needs of the motor response.
Acoustic Stimulation↗
Changes in eye blink responses following hypoglossal-facial anastomosis in the cat: evidence of adult mammal motoneuron unadaptability to new motor tasks.
Hypoglossal-facial anastomosis is used in humans to restore the activity of the mimic musculature following irrecoverable facial nerve lesions. As eyelid movement kinetics is very well known, we have used this experimental model in cats to follow the evolution of blink responses and the adaptability of hypoglossal motor pools to new motor tasks. Although the electromyographic activity of the orbicularis oculi muscle in response to corneal air puffs, flashes of light or electrical stimulation of the supraorbital nerve was not recovered in the seven months following this crossed anastomosis, reflex blinks were got back by the increased activity of the retractor bulbi and extraocular recti muscles. The lid of the anastomosed side oscillated in perfect synchronization with tongue movements during licking, while it was severely affected in its motor function during optokinetic stimulation because of the spontaneous appearance of tongue-related hypoglossal activity. Present results suggest that adult mammal motoneurons are unable to readapt their motor programs to the kinetic needs of new motor targets and that most of the functional recovery observed in the cat was achieved by the compensatory hyperactivity of motor systems not directly affected by the surgery.
Adaptation, Physiological↗
Cerebellar cortex and eyeblink conditioning: bilateral regulation of conditioned responses.
We examined the role of the cerebellum in classical conditioning of the nictitating membrane response (NMR) of rabbits by comparing the effects of unilateral and bilateral cerebellar cortical lesions. Using extended preoperative conditioning to ensure high levels of learning, we confirmed that unilateral lesions of lobules HVI and ansiform lobe impaired conditioned responses (CRs) previously established to an auditory conditioned stimulus, but did not prevent some relearning with post-operative retraining. Bilateral lesions of HVI and ansiform lobe produced similar impairments of CRs, but also prevented subsequent relearning. Unilateral cortical lesions produced significant enhancement of unconditioned response (UR) amplitudes to periorbital electrical stimulation. Bilateral cortical lesions enhanced UR amplitudes to a lesser extent. Because there was no correlation between the degree of CR impairment and UR enhancement across the unilateral and bilateral lesion groups, the suggestion that the lesions impaired CRs due to general effects upon performance, rather than due to losses of learning, is not supported. Both sides of the cerebellar cortex contribute towards learning a unilaterally trained CR. This finding is important for the re-interpretation of unilateral, reversible inactivation studies that have found no involvement of the cerebellar deep nuclei in the acquisition of NMR conditioning. In addition, we found conditioning-dependent modifications of unconditioned responses that were particularly apparent at low intensities of periorbital electrical stimulation. This finding is important for the re-interpretation of studies that have found apparent changes in the UR of conditioned subjects after cerebellar lesions.
Animals↗