Reticulospinal neurons with and without monosynaptic inputs from cerebellar nuclei

1975 ◽  
Vol 38 (3) ◽  
pp. 513-530 ◽  
Author(s):  
J. C. Eccles ◽  
R. A. Nicoll ◽  
W. F. Schwarz ◽  
H. Taborikova ◽  
T. J. Willey

An account is given of the responses of 557 medial reticular neurons with axons projecting down the spinal cord. All 30 experiments were on decerebrated unanesthetized cats paralyzed by Flaxedil. Recording from single neurons was by extracellular glass microelectrodes. Identification was first by location (confirmed by subsequent histology) in the medial reticular nucleus of medulla or pons, and second by antidromic activation from cord stimulation at C2 and L2 segmental levels. Axonal conduction velocities were calculated from the latency differential between L2 and C2 antidromic responses, and were usually in the range of 90-140 m/s; but about 25% were slower, ranging down to 30 m/s. Stimulation by electrodes in the ipsilateral and contralateral fastigial nuclei differentiated reticulospinal neurons into two classes according to whether they did or did not receive monosynaptic inputs, the respective populations of fully investigated neurons being 270 and 174. The fastigioreticular neurons were distinguished by a higher background frequency with mean values of 28 as against 15/s. There were also significant diffences in both the excitatory and inhibitory responses to afferent volleys from forelimb and hindlimb nerves. Comparison of the respective latency histograms showed that the responses of neurons with a fastigial input had an excess of latencies in the ranges that can be correlated with the latency histograms observed for fastigial responses. Thus, there is evidence for the effectiveness of the fastigial input and so for the pathway with monosynaptic linkage: Purkinje cells of cerebellar vermis yields fastigial neurons yields medial reticular neurons projecting down the spinal cord. Adequate stimulation of cutaneous receptors by pad taps and air-jet stimulation of hairy skin in a disppointingly small action when compared with fastigical responses. Explanations of this deficiency are suggested. Another discrpancy from the fastigial responses is that the medial reticular neurons have much wider receptive fields with little discrimination between ipsilateral and contralateral and between forelimb and hindlimb. Stimulation of the ipsilateral tegmental tract was tested on 183 reticulospinal neurons, 112 being with fastigial inputs. In about half there was a powerful monosynaptic excitation, which would identify such neurons as being on the pathway from mesencephalic and diencephalic centers to the spinal cord. There is a general discussion of transmission across successive synaptic relays, where specificity is sacrificed to integration.

1984 ◽  
Vol 51 (3) ◽  
pp. 467-480 ◽  
Author(s):  
W. D. Willis ◽  
K. D. Gerhart ◽  
W. S. Willcockson ◽  
R. P. Yezierski ◽  
T. K. Wilcox ◽  
...  

Recordings were made from 132 raphe- and reticulospinal tract neurons in the medial part of the lower brain stem in 32 anesthetized monkeys. Recording sites were in the nucleus raphe magnus, the rostral nucleus raphe obscurus, and the reticular formation adjacent to the raphe. The neurons were identified by antidromic activation from the upper lumbar spinal cord. Of the population sampled, 83 cells were activated antidromically from the left dorsal lateral funiculus (DLF), 32 from the right DLF, and 17 from both sides. The mean latency for antidromic activation was 8.2 +/- 7.1 ms, corresponding to a mean conduction velocity of 22.8 m/s. No conduction velocities characteristic of unmyelinated axons were observed. Collision tests indicated that raphe-spinal axons that bifurcated to descend in both DLFs branched within the spinal cord. The effects of stimulation in the periaqueductal gray (PAG) or adjacent midbrain reticular formation were tested on 102 spinally projecting neurons in the medial medulla. Of these, 60 cells were excited, 9 cells were inhibited, 8 showed mixed excitation and inhibition, and 25 cells were unaffected. The mean latency for excitation was 11.6 ms and for inhibition, 17.8 ms. Threshold for excitation of raphe- and reticulospinal neurons ranged from 50 to 400 microA. Raphe- and reticulospinal tract cells could often (31/46 cells tested) be excited following stimulation in the ventral posterior lateral nucleus of the thalamus. The mean latency of excitation was 35.6 ms (range, 6-112 ms). Receptive fields could be demonstrated for 80 raphe- and reticulospinal cells, while 48 neurons possessed no demonstrable cutaneous receptive field. Most cells had large excitatory receptive fields, often encompassing the surface of the entire body and face. Some neurons had complex excitatory and inhibitory receptive fields, whereas other cells had large inhibitory receptive fields over much of the surface of the body and face. For most cells (52/55) with excitatory receptive fields, the only effective stimuli were noxious mechanical or noxious heat stimuli. Nonnoxious mechanical stimuli, such as brushing the skin, were capable of activating only a few (3/55) raphe- and reticulospinal neurons, and these were more effectively excited by noxious stimuli.(ABSTRACT TRUNCATED AT 400 WORDS)


1976 ◽  
Vol 39 (1) ◽  
pp. 102-108 ◽  
Author(s):  
J. C. Eccles ◽  
R. A. Nicoll ◽  
D. W. Schwarz ◽  
H. Taborkova ◽  
T. J. Willey

Almost 10% of neurons in the medial reticular nucleus or adjacent thereto were invaded antidromically in response to stimulation of the fastigial and interpositus nuclei. The fraction was 77/835 for the bulbar and caudal pontine levels, but 0/167 for rostral pontine levels. The mahority, 49, of the neurons projecting to the cerebellum were superficially located in the region of the perihypoglossal nucleus, but 23 were scattered through the medial reticular nucleus, being 2.5-5.0 mm below the bulbopontine dorsum. Both classes of cerebellopetal neurons had a similar range of antidromic latencies, usually from 0.8 to 2.0 ms, but some were ober 3 ms. Both classes responded to volleys from limb nerves and inputs from cutaneous mechanoreceptors, with ranges of excitatory and inhibitory latencies that were similar to those for other medial reticular neurons. It is conjectured that the axonal projection is primarily to the cerebellar cortex and that the branches to the nuclei are often slender, hence the long antidromic latencies; 31 of 59 neurons tested projected to cerebellar nuclei on both sides, often with a considerable latency differential. Rarely, there were also axonal branches projecting up the central tegmental tract. The experimental findings are in very good accord with the anatomical descriptions of Brodal and associates (4, 5, 8, 19). It is suggested that the paramedian reticular and the perihypoglossal nuclei may provide a background excitatory input to the interpositus nuclei.


1987 ◽  
Vol 58 (4) ◽  
pp. 719-738 ◽  
Author(s):  
S. M. Highstein ◽  
J. M. Goldberg ◽  
A. K. Moschovakis ◽  
C. Fernandez

1. Intracellular recordings were made from secondary neurons in the vestibular nuclei of barbiturate-anesthetized squirrel monkeys. Monosynaptic excitatory postsynaptic potentials (EPSPs) evoked by stimulation of the ipsilateral vestibular nerve (Vi) were measured. An electrophysiological paradigm, described in the preceding paper (26), was used to determine the proportion of irregularly (I) and regularly (R) discharging Vi afferents making direct connections with individual secondary neurons. The results were expressed as a % I index, an estimate for each neuron of the percentage of the total Vi monosynaptic input that was derived from I afferents. The secondary neurons were also classified as I, R, or M cells, depending on whether they received their direct Vi inputs predominantly from I or R afferents or else from a mixture (M) of both kinds of Vi fibers. The neurons were located in the superior vestibular nucleus (SVN) or in the rostral parts of the medical or lateral (LVN) vestibular nuclei. 2. Antidromic activation or reconstruction of axonal trajectories after intrasomatic injection of horseradish peroxidase (HRP) was used to identify three classes of secondary neurons in terms of their output pathways: 1) cerebellar-projecting (Fl) cells innervating the flocculus (n = 26); 2) rostrally projecting (Oc) cells whose axons ascended toward the oculomotor (IIIrd) nucleus (n = 27); and 3) caudally projecting (Sp) cells with axons descending toward the spinal cord (n = 13). Two additional neurons, out of 21 tested, could be antidromically activated both from the level of the IIIrd nucleus and from the spinal cord. 3. The Vi inputs to the various classes of relay neurons differed. As a class, Oc neurons received the most regular inputs. Sp neurons had more irregular inputs. Fl neurons were heterogeneous with similar numbers of R, M, and I neurons. The mean values (+/- SD) of the % I index for the Oc, Fl, and Sp neurons were 34.7 +/- 24.7, 51.9 +/- 30.4, and 61.8 +/- 18.0%, respectively. Only the Oc neurons had a % I index that was similar to the proportion of I afferents (34%) in the vestibular nerve (cf. Ref. 26). 4. The commissural inputs from the contralateral vestibular nerve (Vc) also differed for the three projection classes. Commissural inhibition was most common in Fl cells: 22/25 (88%) of the neurons had Vc inhibitory postsynaptic potentials (IPSPs) and 1/25 (4%) had a Vc EPSP. In contrast, Vc inputs were only observed in approximately half the Oc and Sp neurons.(ABSTRACT TRUNCATED AT 400 WORDS)


1990 ◽  
Vol 64 (4) ◽  
pp. 1134-1148 ◽  
Author(s):  
S. N. Currie ◽  
P. S. Stein

1. We demonstrated multisecond increases in the excitability of the rostral-scratch reflex in the turtle by electrically stimulating the shell at sites within the rostral-scratch receptive field. To examine the cellular mechanisms for these multisecond increases in scratch excitability, we recorded from single cutaneous afferents and sensory interneurons that responded to stimulation of the shell within the rostral-scratch receptive field. A single segment of the midbody spinal cord (D4, the 4th postcervical segment) was isolated in situ by transecting the spinal cord at the segment's anterior and posterior borders. The isolated segment was left attached to its peripheral nerve that innervates part of the rostral-scratch receptive field. A microsuction electrode (4-5 microns ID) was used to record extracellularly from the descending axons of cutaneous afferents and interneurons in the spinal white matter at the posterior end of the D4 segment. 2. The turtle shell is innervated by slowly and rapidly adapting cutaneous afferents. All cutaneous afferents responded to a single electrical stimulus to the shell with a single action potential. Maintained mechanical stimulation applied to the receptive field of some slowly adapting afferents produced several seconds of afterdischarge at stimulus offset. We refer to the cutaneous afferent afterdischarge caused by mechanical stimulation of the shell as "peripheral afterdischarge." 3. Within the D4 spinal segment there were some interneurons that responded to a brief mechanical stimulus within their receptive fields on the shell with short afterdischarge and others that responded with long afterdischarge. Short-afterdischarge interneurons responded to a single electrical pulse to a site in their receptive fields either with a brief train of action potentials or with a single action potential. Long-afterdischarge interneurons responded to a single electrical shell stimulus with up to 30 s of afterdischarge. Long-afterdischarge interneurons also exhibited strong temporal summation in response to a pair of electrical shell stimuli delivered up to several seconds apart. Because all cutaneous afferents responded to an electrical shell stimulus with a single action potential, we conclude that electrically evoked afterdischarge in interneurons was produced by neural mechanisms in the spinal cord; we refer to this type of afterdischarge as "central afterdischarge." 4. These results demonstrate that neural mechanisms for long-lasting excitability changes in response to cutaneous stimulation reside in a single segment of the spinal cord. Cutaneous interneurons with long afterdischarge may serve as cellular loci for multise


1988 ◽  
Vol 60 (6) ◽  
pp. 1967-1981 ◽  
Author(s):  
W. S. Ammons

1. Studies were done to characterize responses of spinal neurons backfired from the ventrolateral medulla to renal and somatic stimuli. Experiments were performed on 31 cats that were anesthetized with alpha-chloralose. Sixty-six spinal neurons were antidromically activated from the area of the lateral reticular nucleus or the ventrolateral reticular formation just rostral to the lateral reticular nucleus contralateral to the recording site. These cells could not be backfired from the medial reticular formation or from the spinothalamic tract just caudal to the thalamus. 2. Cells were located in laminae I, V, and VII of the T12-L2 segments. Antidromic conduction velocities averaged 35.9 +/- 7.2 m/s. Conduction velocities were unrelated to the projection site or laminar location of the cells. Termination sites of 21 cells were located in antidromic mapping experiments. Terminals were localized to the ventrolateral reticular formation, including the lateral reticular nucleus. 3. Responses to electrical stimulation of the renal nerves were always excitatory. Stimulation of renal A-delta-fibers excited 33 cells. These cells failed to respond to stimulation of renal C-fibers. The other 33 cells responded to both A-delta- and C-fiber stimulation. Latencies to A-delta-fiber stimulation averaged 9 +/- 2 ms, whereas latencies to C-fiber stimulation averaged 57 +/- 10 ms. 4. Renal mechanoreceptors were activated by occlusion of the renal vein or upper portion of the ureter. Renal vein occlusion excited 14 of 32 cells tested. Activity increased from 6 +/- 2 to 14 +/- 4 spike/s. Ureteral occlusion increased activity of 19 of 32 cells from 7 +/- 2 to 16 +/- 5 spikes/s. Cells responding to one of the mechanical stimuli were significantly more likely to receive A-delta-and C-fiber input compared with nonresponding cells. Nonresponders were more likely than responders to receive only A-delta input. 5. All cells received somatic input in addition to renal input. Twelve cells were classified as wide dynamic range, 46 as high threshold, and 8 as Deep. Somatic receptive fields most often included skin and muscle of the left flank and abdomen. Thirty-two cells had bilateral receptive fields, and 22 had inhibitory fields in addition to excitatory fields. 6. These data show that spinal neurons projecting to the ventrolateral medulla receive convergent inputs from the kidney and somatic structures. These cells may participate in a variety of functions including autonomic reflexes of renal origin.


1978 ◽  
Vol 41 (3) ◽  
pp. 821-834 ◽  
Author(s):  
P. W. Wyzinski ◽  
R. W. McCarley ◽  
J. A. Hobson

1. Reticulospinal neurons were identified by antidromic invasion from spinal cord electrodes chronically implanted at C4 in cats. 2. Most of the neuronal population studied lay within the medial portion of the giant cell field from the anterior pontine and to the anterior medullary reticular formation (FTG). A few cells were found in the tegmental reticular nucleus (TRC) which has not previously been known to project to the spinal cord. 3. Extracellular action potentials from the neuronal somata of the identified neurons were recorded continuously throughout naturally occurring sleep-waking cycles. 4. The identified reticulospinal neurons shared three properties, suggesting a generator function in desynchronized sleep (D) (with previously recorded but unidentified FTG neurons): selectivity (or concentration of discharge in D); tonic latency (or firing rate increases beginning several minutes prior to D); and phasic latency (or firing rate increases occurring prior to eye movements within D). 5. The location, discharge properties, and spinal projections of FTG neurons are, thus, all consistent with the hypothesis that they may directly mediate some of the descending excitatory and inhibitory influences on spinal reflex pathways in desynchronized sleep.


2020 ◽  
Author(s):  
Iliodora V. Pop ◽  
Felipe Espinosa ◽  
Megan Goyal ◽  
Bishakha Mona ◽  
Mark A. Landy ◽  
...  

AbstractProprioception, the sense of limb and body position, generates a map of the body that is essential for proper motor control, yet we know little about precisely how neurons in proprioceptive pathways develop and are wired. Proprioceptive and cutaneous information from the periphery is sent to secondary neurons in the spinal cord that integrate and relay this information to the cerebellum either directly or indirectly through the medulla. Defining the anatomy of these direct and indirect pathways is fundamental to understanding how proprioceptive circuits function. Here, we use genetic tools in mice to define the developmental origins and unique anatomical trajectories of these pathways. Developmentally, we find that Clarke’s column (CC) neurons, a major contributor to the direct spinocerebellar pathway, derive from the Neurog1 progenitor domain. By contrast, we find that two of the indirect pathways, the spino-lateral reticular nucleus (spino-LRt) and spino-olivary pathways, are derived from the Atoh1 progenitor domain, despite previous evidence that Atoh1-lineage neurons form the direct pathway. Anatomically, we also find that the mossy fiber terminals of CC neurons diversify extensively with some axons terminating bilaterally in the cerebellar cortex. Intriguingly, we find that CC axons do not send axon collaterals to the medulla or cerebellar nuclei like other mossy fiber sources. Altogether, we conclude that the direct and indirect spinocerebellar pathways derive from distinct progenitor domains in the developing spinal cord and that the proprioceptive information from CC neurons is processed only at the level of granule cells in the cerebellum.Significance StatementWe find that a majority of direct spinocerebellar neurons in mice originate from Clarke’s column (CC), which derives from the Neurog1-lineage, while few originate from Atoh1-lineage neurons as previously thought. Instead, we find that spinal cord Atoh1-lineage neurons form mainly the indirect spino-lateral reticular nucleus and spino-olivary tracts. Moreover, we observe that mossy fiber axon terminals of CC neurons diversify proprioceptive information across granule cells in multiple lobules on both ipsilateral and contralateral sides without sending axon collaterals to the medulla or cerebellar nuclei. Altogether, we define the development and the anatomical projections of direct and indirect pathways to the cerebellum from the spinal cord.


1989 ◽  
Vol 62 (2) ◽  
pp. 487-494 ◽  
Author(s):  
P. Zarzecki

1. Multiple output pathways originate from motor cortex. In this study on cats, six classes of corticofugal neurons were identified by antidromic activation. Corticocallosal neurons of layer III were activated antidromically by stimulation of contralateral motor cortex. Layer V neurons were identified by antidromic activation from cerebral peduncle, red nucleus, lateral reticular nucleus of medulla, or spinal cord. Corticothalamic neurons were identified in layer VI. All the identified neurons were tested for input from primary somatosensory cortex. 2. Neurons of all corticofugal groups received excitatory inputs from primary somatosensory cortex. The shortest latency corticocortical effects of 1.2-2.5 ms were found for corticocallosal neurons of layer III, and for layer V neurons which projected axons through the cerebral peduncle, to red nucleus, and to spinal cord. 3. Nearby neurons, projecting to the same of different targets, were affected nonuniformly by corticocortical inputs. This finding supports the conclusion that specificity of afferent connections within cerebral cortex is not determined by anatomic segregation of cell bodies nor by projection target of efferent neurons. 4. These selectively distributed input connectivities suggest that even a small region of motor cortex could send different signals to its diverse targets.


2000 ◽  
Vol 84 (4) ◽  
pp. 2078-2112 ◽  
Author(s):  
Amy Malick ◽  
Rew M. Strassman ◽  
Rami Burstein

Sensory information that arises in orofacial organs facilitates exploratory, ingestive, and defensive behaviors that are essential to overall fitness and survival. Because the hypothalamus plays an important role in the execution of these behaviors, sensory signals conveyed by the trigeminal nerve must be available to this brain structure. Recent anatomical studies have shown that a large number of neurons in the upper cervical spinal cord and caudal medulla project directly to the hypothalamus. The goal of the present study was to identify the types of information that these neurons carry to the hypothalamus and to map the route of their ascending axonal projections. Single-unit recording and antidromic microstimulation techniques were used to identify 81 hypothalamic-projecting neurons in the caudal medulla and upper cervical (C1) spinal cord that exhibited trigeminal receptive fields. Of the 72 neurons whose locations were identified, 54 were in laminae I–V of the dorsal horn at the level of C1 ( n = 22) or nucleus caudalis (Vc, n = 32) and were considered trigeminohypothalamic tract (THT) neurons because these regions are within the main projection territory of trigeminal primary afferent fibers. The remaining 18 neurons were in the adjacent lateral reticular formation (LRF) and were considered reticulohypothalamic tract (RHT) neurons. The receptive fields of THT neurons were restricted to the innervation territory of the trigeminal nerve and included the tongue and lips, cornea, intracranial dura, and vibrissae. Based on their responses to mechanical stimulation of cutaneous or intraoral receptive fields, the majority of THT neurons were classified as nociceptive (38% high-threshold, HT, 42% wide-dynamic-range, WDR), but in comparison to the spinohypothalamic tract (SHT), a relatively high percentage of low-threshold (LT) neurons were also found (20%). Responses to thermal stimuli were found more commonly in WDR than in HT neurons: 75% of HT and 93% of WDR neurons responded to heat, while 16% of HT and 54% of WDR neurons responded to cold. These neurons responded primarily to noxious intensities of thermal stimulation. In contrast, all LT neurons responded to innocuous and noxious intensities of both heat and cold stimuli, a phenomenon that has not been described for other populations of mechanoreceptive LT neurons at spinal or trigeminal levels. In contrast to THT neurons, RHT neurons exhibited large and complex receptive fields, which extended over both orofacial (“trigeminal”) and extracephalic (“non-trigeminal”) skin areas. Their responses to stimulation of trigeminal receptive fields were greater than their responses to stimulation of non-trigeminal receptive fields, and their responses to innocuous stimuli were induced only when applied to trigeminal receptive fields. As described for SHT axons, the axons of THT and RHT neurons ascended through the contralateral brain stem to the supraoptic decussation (SOD) in the lateral hypothalamus; 57% of them then crossed the midline to reach the ipsilateral hypothalamus. Collateral projections were found in the superior colliculus, substantia nigra, red nucleus, anterior pretectal nucleus, and in the lateral, perifornical, dorsomedial, suprachiasmatic, and supraoptic hypothalamic nuclei. Additional projections (which have not been described previously for SHT neurons) were found rostral to the hypothalamus in the caudate-putamen, globus pallidus, and substantia innominata. The findings that nonnociceptive signals reach the hypothalamus primarily through the direct THT route, whereas nociceptive signals reach the hypothalamus through both the direct THT and the indirect RHT routes suggest that highly prioritized painful signals are transferred in parallel channels to ensure that this critical information reaches the hypothalamus, a brain area that regulates homeostasis and other humoral responses required for the survival of the organism.


1998 ◽  
Vol 79 (2) ◽  
pp. 964-982 ◽  
Author(s):  
Rami Burstein ◽  
Hiroyoshi Yamamura ◽  
Amy Malick ◽  
Andrew M. Strassman

Burstein, Rami, Hiroyoshi Yamamura, Amy Malick, and Andrew M. Strassman. Chemical stimulation of the intracranial dura induces enhanced responses to facial stimulation in brain stem trigeminal neurons. J. Neurophysiol. 79: 964–982, 1998. Chemical activation and sensitization of trigeminal primary afferent neurons innervating the intracranial meninges have been postulated as possible causes of certain headaches. This sensitization, however, cannot explain the extracranial hypersensitivity that often accompanies headache. The goal of this study was to test the hypothesis that chemical activation and sensitization of meningeal sensory neurons can lead to activation and sensitization of central trigeminal neurons that receive convergent input from the dura and skin. This hypothesis was investigated by recording changes in the responsiveness of 23 [16 wide-dynamic range (WDR), 5 high threshold (HT), and 2 low threshold (LT)] dura-sensitive neurons in nucleus caudalis to mechanical stimulation of their dural receptive fields and to mechanical and thermal stimulation of their cutaneous receptive fields after local application of inflammatory mediators or acidic agents to the dura. Responses to brief chemical stimulation were recorded in 70% of the neurons; most were short, lasting the duration of the stimulus only. Twenty minutes after chemical stimulation of the dura, the following changes occurred: 1) 95% of the neurons showed significant increases in sensitivity to mechanical indentation of the dura: their thresholds to dural indentation changed from 1.57 to 0.49 g (means, P < 0.0001), and the response magnitude to identical stimuli increased by two- to fourfold; 2) 80% of the neurons showed significant increases in cutaneous mechanosensitivity: their responses to brush and pressure increased 2.5- ( P < 0.05) and 1.6-fold ( P < 0.05), respectively; 3) 75% of the neurons showed a significant increase in cutaneous thermosensitivity: their thresholds to slow heating of the skin changed from 43.7 ± 0.7 to 40.3 ± 0.7°C ( P < 0.005) and to slow cooling from 23.7 ± 3.3 to 29.2 ± 1.8°C ( P < 0.05); 4) dural receptive fields expanded within 30 min and cutaneous receptive fields within 2–4 h; and 5) ongoing activity developed in WDR and HT but not in LT neurons. Application of lidocaine to the dura abolished the response to dural stimulation but had minimal effect on the increased responses to cutaneous stimulation (suggesting involvement of a central mechanism in maintaining the sensitized state). Antidromic activation (current of <30 μA) of dura-sensitive neurons revealed projections to the hypothalamus, thalamus, and midbrain. These findings suggest that chemical activation and sensitization of dura-sensitive peripheral nociceptors could lead to enhanced responses in central neurons and that this central sensitization therefore could result in extracranial tenderness (mechanical and thermal allodynia) in the absence of extracranial pathology. The projection targets of these neurons suggest a possible role in mediating the autonomic, endocrine, and affective symptoms that accompany headaches.


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