Philip M. Groves

Self-inhibition by dopaminergic neurons.

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Spontaneous firing patterns of identified spiny neurons in the rat neostriatum

Spontaneous firing patterns of 94 unidentified neurons and 34 identified spiny neurons were compared in the neostriatum of locally anesthetized immobilized rats. Intracellular and extracellular recordings were analyzed using first order interval histograms and autocorrelograms, and neurons were identified by their somatodendritic morphology after intracellular injection of horseradish peroxidase. All neostriatal neurons tended to fire in irregular phasic bursts of activity. Considerable variation in mean firing rate, burst duration, interburst interval and the occurrence and rate of firing between bursts was apparent in both groups of neurons. There was no apparent difference between spiny neurons and the sample of unidentified extracellularly recorded neurons along any of these firing pattern parameters. Intracellular recordings from identified spiny neurons revealed noisy irregular periods of maintained 5-20 mV membrane depolarizations which corresponded to the occurrence of bursts of firing in spontaneously active neurons. These depolarizations occurred in neostriatal neurons exhibiting no spontaneous activity but were of insufficient amplitude to trigger impulse activity.

Monoaminergic synapses, including dendro-dendritic synapses in the rat substantia nigra

SummaryIntraventricular administration of 1 or 2 mg of the osmiophilic “false transmitter” 5-hydroxydopamine (5-OHDA) was used to label monoamine storage and release sites in the rat substantia nigra. Vesicles containing unusually dense cores indicative of the presence of the marker were seen forming from the Golgi apparatus in the cell bodies of medium-sized neurons of the substantia nigra, pars compacta, and from smooth endoplasmic reticulum in the dendrites of those neurons and in small unmyelinated axons of unknown origin. In serial sections, both axons and dendrites containing synaptic vesicles marked with 5-OHDA were seen to form synapses “en passage” in pars compacta, and some presynaptic dendrites containing vesicles filled by the marker were also observed to form contacts with dendrites in pars reticulata. The only identified postsynaptic elements engaging in monoaminergic synapses in the substantia nigra were dendrites of medium-sized pars compacta neurons.

Dopamine receptor changes following destruction of the nigrostriatal pathway: Lack of a relationship to rotational behavior

Phenomena consistent with postsynaptic supersensitivity developed in the rat neostriatum following the destruction of dopaminergic afferent neurons. A gradual increase in the density of binding sites for [3H]spiperone occurred over a 2-3 week period. This increase was apparent only after the almost complete loss of dopamine-containing nerve terminals as measured by the depletion of endogenous dopamine. The properties of the receptor labeled by [3H]spiperone were not altered by denervation. Elimination of dopamine-containing nerve endings in the neostriatum was accompanied by the gradual development of an increase in dopamine-sensitive adenylate cyclase activity in homogenates of the caudate ipsilateral to the lesion as compared to the contralateral side. The administration of apomorphine led to pronounced circling behavior. This effect occurred rapidly and was maximal within 3 days following destruction of dopaminergic neurons. The increase in the density of dopamine receptors and in a receptor-mediated function may partially account for the development of enhanced electrophysiological responses to dopamine agonists in the neostriatum. However, the results do not explain the drug-induced rotational behavior which develops after destruction of the dopamine-containing nigrostriatal pathway. This behavioral phenomenon clearly preceded the appearance of receptor alterations in the corpus striatum.

Statistical properties of neuronal spike trains in the substantia nigra: cell types and their interactions.

Summary Spike trains from spontaneously active neurons in the substantia nigra of locally anesthetized, immobilized rats could be included in one of three broad categories, on the basis of the form of their autocorrelation histograms and spike waveforms. Initial brief trough (IBT) cells show a tendency not to fire for 10–50 msec after generation of an action potential. The duration of this period, which is seen as an initial trough in the auto-correlation histogram, is inversely related to firing rate for these neurons. Cells of this type fire repetitively at rates above 15–20/sec, and are found predominantly in the pars reticulata of the substantia nigra. Initial prolonged trough (IPT) cells have substantially longer initial troughs (60–250 msec) in their auto-correlation histograms, from which firing probability recovers more gradually. IPT cells have a trough length which increases with increasing firing rate for rates below 3–6/sec, the threshold for repetitive firing. They are found in the pars compacta and probably represent the dopaminergic neurons of that area. Bursty cells are much less numerous than cells of the other types, and are found in both parts of the substantia nigra, although about twice as commonly in pars reticulata. They fire in bursts of variable length, and may represent nigral interneurons. Cross-correlations between these different cell types suggest several potential synaptic interactions between neurons intrinsic to the substantia nigra. In addition, the possibility of shared excitatory or inhibitory input to different classes of neurons in the substantia nigra is discussed, as well as the relation of these statistical properties to neuropharmacological and anatomical observations on neurons of the substantia nigra.

Brain stem pathways, cortical modulation, and habituation of the acoustic startle response.

Rats with bilateral lesions in the inferior colliculi, superior colliculi, anterior (mesencephalic) reticular formation, or posterior (pontine) reticular formation, in addition to sham-operated animals, were studied to determine the effects of damage to these sites on short-term (within sessions) or long-term (across days) habituation of the acoustic startle response. Lesions placed in posterior reticular formation reduced short-term habituation, while damage to other structures had little effect. Damage to the inferior colliculi, anterior reticular formation, and posterior reticular formation reduced or abolished long-term habituation. In addition, damage to the inferior colliculi abolished the acoustic startle response for 2 to 3 days postoperatively, but full recovery of the response was evident by 4-days postoperative recovery. Startle response amplitude was related to the anterior-posterior placement of reticular formation lesions. More posteriorly placed lesions reduced or abolished the startle response. These results suggest that the reticular formation may underlie short-term habituation of the acoustic startle response and that the normal pathway of this response involves information relayed to reticular formation via the inferior colliculi. However, parallel pathways from lower auditory relay appear to exist since complete recovery of the acoustic startle occurs within 4 days following removal of the inferior colliculi. Rats with lesions in the frontal poles, dorsal hippocampus and overlying parietal cortex, parietal cortex alone, or auditory cortex were studied to determine the effects of damage to these areas on short-term or long-term habituation of the acoustic startle response. With the exception of parietal cortical control lesions, all subjects showed some impairment of long-term habituation following cortical damage. Short-term habituation was unaffected by any of the lesions. The results are compared to previous reports of the effects of damage to cortex and the brain stem.

Organization by sensory modality in the reticular formation of the rat

Abstract The activity of 304 neurons in the reticular formation of the rat, extending from the anterior border of the superior colliculus to the entrance of the eighth cranial nerve, was recorded using extracellular microelectrodes. Approximately one-half of the neurons in our sample did not respond to sensory stimulation (auditory, visual or tactile stimuli), while others responded to visual, auditory or tactile stimuli singly or in various combinations. Cells responding to visual stimulation were located in the anterior mesencephalic reticukar formation, below the superior colliculus. Cells responsive to auditory stimulation were located in the region adjacent to the inferior colliculus and nucleus of the lateral lemniscus, while cells responsive to tactile stimulation were evenly distributed throughout the reticular formation. Receptive fields of tactile cells were quite large. Cells having receptive fields confined to the anterior, middle or posterior third of the body surface were distributed within the reticular formation according to a regional somatotopic organization. Cells responding to the anterior third of the body were located in the anterior reticular formation or the extreme posterior reticular formation at the level of the nucleus of the trigeminal nerve. Cells responding to the middle third of the body surface were located in the posterior mesencephalic and anterior pontine reticular formation, and cells responding to the posterior third of the body were located in the posterior aspect of the reticular formation. Cells responsive to more than one modality were distributed primarily in the mesencephalon. These distributions of sensory responses were discussed in terms of the known anatomical distributions of reticular afferents.

Amphetamine-induced release of dopamine from the substantia nigra in vitro

Incubation of chopped tissue from the substantia nigra of the rat brain with d-amphetamine resulted in a significant release of [3H]dopamine into the incubation medium. This effect was observed with both exogenous [3H]dopamine previously taken up by the tissue and [3H]dopamine endogenously synthesized from L-[3,5-3H]tyrosine. The observed release was greater in magnitude when the apparent conversion of released dopamine to 3-methoxytyramine was taken into account. The relevance of the present results to the previously postulated self-inhibition by dopaminergic neurons of the substantia nigra pars compacta is discussed. The present data also provide support for the concept that catechol-O-methyltransferase (E.C.2.1.1.6.) is located primarily extraneuronally in brain.

A simple and rapid section embedding technique for sequential light and electron microscopic examination of individually stained central neurons

A method for section embedding of central nervous tissue, and its application to light and electron microscopic examination of neurons stained by intracellular injection of horseradish peroxidase, is described. After primary fixation in aldehydes, thick (10--80 micrometer) sections are cut on a Vibratome. They are then treated for the histochemical demonstration of peroxidase, postfixed in osmium tetroxide, dehydrated and infiltrated with Spurrs low viscosity resin. Infiltrated sections are embedded between glass slides and coverslips coated with a transparent layer of teflon and polymerized. The resulting mount allows protracted storage and high resolution light microscopic examination of sections. When desired, the glass components can be removed and the specimen cemented to a blank block for thin sectioning and electron microscopic examination.

Sensory evoked neuronal activity in the hippocampus before and after lesions of the medial septal nuclei.

Abstract The evoked activity of 142 single neurons in the hippocampus of 44 rats was recorded following presentation of one of several modalities of peripheral stimulation. In the intact rat, 41% of the neurons encountered showed some period of inhibition of neuronal firing following peripheral stimulation. In subjects that had received lesions of the medial septal nuclei, only 21% of the cells encountered showed such inhibition. Medial septal lesions were made in 23 animals while recording the activity of cells which exhibited inhibition following stimulation. Of these 23 cells, only 5 continued to exhibit response inhibition after the lesion, while 13 displayed only response excitation, and 5 showed a complete loss of responsiveness. These findings suggest that the integrity of the medial septal nucleus is necessary for the inhibition of neuronal firing observed in many hippocampal neurons following peripheral stimulation.