Quantitative analysis of central terminal projections of visceral and somatic unmyelinated (C) primary afferent fibers in the guinea pig

Sugiura, Yasuo; Terui, Naohito; Hosoya, Yoshinori; Tonosaki, Yoshikazu; Nishiyama, Keiji; Honda, Takashi

doi:10.1002/cne.903320305

Cited by 57 publications

(34 citation statements)

References 80 publications

Supporting

Mentioning

Contrasting

Unclassified

Order By: Relevance

“…C fibers from muscle coursed through the DF (and not through Lissauer's tract, as previously believed), with collaterals emanating over three segments and more, exhibiting a substantial termination in the white matter dorsal to lamina I. These fibers could provide inputs to the poorly defined neurons occasionally reported for the DF (Mizumura et al, 1993;Sugiura et al, 1993).…”

Section: Differential Termination Of Muscle Afferent Fibersmentioning

confidence: 71%

Central projection of unmyelinated (C) primary afferent fibers from gastrocnemius muscle in the guinea pig

Ling

Honda

Shimada

et al. 2003

J of Comparative Neurology

View full text Add to dashboard Cite

We have demonstrated the central projections of muscle C or group IV afferent fibers in the guinea pig by tracing arborizations in the spinal cord. C afferent fibers from the gastrocnemius muscle (GCM) were electrophysiologically identified by conduction velocity (less than 1 m/second). A single neuron in the lumbar 5 dorsal root ganglion (L5 DRG) was intracellularly labeled with Phaseolus vulgaris leucoagglutinin (PHA-L). After iontophoretic injection of PHA-L, we processed the lumbar cord and L5 DRG for PHA-L immunohistochemistry. Six muscle C afferent fibers from 40 animals were labeled, and whole trajectories were recovered. Labeled fibers were reconstructed by tracing of the arbor in serial parasagittal sections. The GCM C afferents projected rostrocaudally for two or three segments and ran at the surface of the dorsal funiculus, giving off collaterals into laminae I and II and sometimes into parts of lamina III. We determined, based on the branching pattern and form of the terminal plexus, that the branching of muscle C afferent fibers showed an intermediate pattern that fell morphologically between the terminal patterns of somatic and visceral afferents. The numbers and sizes of fiber swellings and terminal swellings were measured on all collateral branches. We found that the area of distribution of the terminal swellings of muscle C afferent fibers is larger than that of somatic terminals but that the density of terminal swellings in the terminal area was lower than that of the somatic terminals.

show abstract

Section: Differential Termination Of Muscle Afferent Fibersmentioning

confidence: 71%

Central projection of unmyelinated (C) primary afferent fibers from gastrocnemius muscle in the guinea pig

Ling

Honda

Shimada

et al. 2003

J of Comparative Neurology

View full text Add to dashboard Cite

show abstract

“…Lamina II neurons receive inputs from A␦-and C-fiber nociceptors as well as innocuous thermal receptors and mechanoreceptors (Light and Perl 1979b;Sugiura et al 1986Sugiura et al , 1993. Because these thin fibers are often involved in nociception, lamina II is presumed to be a critical center in pain mechanisms.…”

Section: Discussionmentioning

confidence: 99%

Primary Afferent Stimulation Differentially Potentiates Excitatory and Inhibitory Inputs to Spinal Lamina II Outer and Inner Neurons

Pan

Pan²

2004

Journal of Neurophysiology

View full text Add to dashboard Cite

Pan, Yu-Zhen and Hui-Lin Pan. Primary afferent stimulation differentially potentiates excitatory and inhibitory inputs to spinal lamina II outer and inner neurons. J Neurophysiol 91: 2413-2421, 2004. First published January 28, 2004 10.1152/jn.01242.2003. Spinal lamina II (substantia gelatinosa) neurons play an important role in processing of nociceptive information from primary afferent nerves. Anatomical studies suggest that neurons in the outer (lamina II o ) and inner (lamina II i ) zone of lamina II receive distinct afferent inputs. The functional significance of this preferential afferent termination in lamina II remains unclear. In this study, we examined the differential synaptic inputs to neurons in lamina II o and II i in response to primary afferent stimulation. Whole cell voltage-clamp recordings were performed on neurons in lamina II o and II i of the rat spinal cord slice under visual guidance. Capsaicin (1 M) significantly increased the frequency of glutamatergic miniature excitatory postsynaptic currents (mEPSCs) in all 27 lamina II o neurons and significantly increased the amplitude of mEPSCs in 12 of 27 lamina II o neurons. However, capsaicin only significantly increased the frequency of mEPSCs in 9 of 22 (40.9%) lamina II i neurons and increased the amplitude of mEPSCs in 6 of these 9 neurons. Furthermore, the peak amplitude of EPSCs, evoked by electrical stimulation of the attached dorsal root, in 40 lamina II o neurons was significantly greater than that [160.5 Ϯ 16.7 vs. 87.0 Ϯ 10.4 (SE) pA] in 37 lamina II i neurons. On the other hand, the peak amplitude of evoked inhibitory postsynaptic currents (IPSCs) in 40 lamina II o neurons was significantly smaller than that (103.1 Ϯ 11.6 vs. 258.4 Ϯ 24.4 pA) in 37 lamina II i neurons. In addition, the peak amplitudes of both EPSCs and IPSCs, evoked by direct stimulation of lamina II, were similar in lamina II o and II i neurons. This study provides new information that stimulation of primary afferents differentially potentiates synaptic inputs to neurons in lamina II o and II i . The quantitative difference in excitatory and inhibitory synaptic inputs to lamina II o and II i neurons may be important for integration of sensory information from primary afferent nerves. I N T R O D U C T I O NLamina II (substantia gelatinosa) of the spinal cord dorsal horn is a critical site for the relay and processing of primary afferent information (Cervero and Iggo 1980; Light and Perl 1979a;Ralston and Ralston 1979;Woolf and Fitzgerald 1983). With a high density of small interneurons and mostly unmyelinated and thinly myelinated primary afferent terminals, lamina II appears to be a heterogenous region both structurally and functionally. Anatomical studies have divided lamina II into two general subdivisions: an outer lamina II (lamina II o ) with small cells and unmyelinated C-fiber terminals and an inner lamina II (lamina II i ) with slightly larger neurons and predominately thinly myelinated A-fiber endings (Light and Perl 1979a,b;Woodbury et al. 2000). Lam...

show abstract

“…Both trigeminal primary sensory neurons and lamina II neurons were consistently labeled within 24 hr after the first appearance of PRV immunoreactivity in neurons of lamina I, providing evidence that lamina I projection cells receive direct input from both primary afferents and from underlying lamina II cells (Gobel, 1978a,b;Hoheisel and Mense, 1989;Sugiura et al, 1993). Double labeling of trigeminal ganglion neurons for PRV and substance P suggests that these lamina I projection neurons are acted on by peptide-containing nociceptive primary afferents, consistent with recent reports (Ding et al, 1995a,b) demonstrating that some lamina I neurons that project to the parabrachial complex express the substance P receptor.…”

Section: Transneuronal Labeling Of Inputs To the Lamina I Projection mentioning

confidence: 92%

Transneuronal Labeling of a Nociceptive Pathway, the Spino-(Trigemino-)Parabrachio-Amygdaloid, in the Rat

et al. 1997

View full text Add to dashboard Cite

Transneuronal tracing of a nociceptive pathway, the spino-(trigemino)-parabrachio-amygdaloid pathway, was performed using an ␣-herpes virus, the Bartha strain of pseudorabies virus (PRV). Microinjection of PRV into the central nucleus of the amygdala (Ce) resulted in progressive retrograde and transneuronal infection of a multisynaptic circuit involving neurons in the brainstem and spinal cord as detected immunocytochemically. At short survival (26 hr), retrogradely labeled neurons were concentrated in the external lateral nucleus of the parabrachial complex (elPB) but were absent from both the trigeminal nucleus caudalis (TNC) and the spinal cord. At longer survivals (52 hr), labeled cells were present in lamina I of both the TNC and spinal dorsal horn. Retrograde labeling from the Ce with Fluorogold demonstrated that elPB neurons have long dendrites extending laterally into the terminal field of spinal and trigeminal afferents, where transneuronal passage of PRV to these afferents could occur. Even longer survivals (76 hr) resulted in a columnar pattern of cell labeling in the TNC and spinal dorsal horn that extended from lamina I into lamina II. At this longest survival, primary sensory neurons became infected. Bilateral excitotoxic lesions of the elPB blocked almost all viral passage from the Ce to superficial laminae of the TNC and spinal dorsal horn. These results demonstrate that nociceptive input to the amygdala is relayed from neurons in lamina I through the elPB. We propose that this modular arrangement of lamina I and II neurons may provide the basis for spinal processing of peripheral input to the amygdala. Key words: pain pathways; amygdala; superficial dorsal horn; parabrachial nucleus; spinal processing; viral tracer; PRV; pseudorabies virusThe central nucleus of the amygdala (Ce) is the terminal area of a major ascending nociceptive pathway, the spino-(trigemino)-parabrachio-amygdaloid tract . Most Ce neurons respond to noxious, but not innocuous, stimuli (Bernard and Besson, 1990;. The main source of afferents to the Ce is the external lateral parabrachial nucleus (elPB) (Saper, 1995). Previous anatomical studies have, however, failed to demonstrate a significant projection from the spinal dorsal horns and trigeminal nucleus caudalis (TNC) to the elPB (Blomqvist et al., 1989). Rather, afferents from nociceptive regions of the dorsal horn, laminae I and V, terminate in nuclei located in the lateral parabrachial area surrounding the elPB, none of which project to the amygdala (Bernard et al., 1995;Feil and Herbert, 1995;Saper, 1995).To explain this discrepancy, it has been proposed that elPB neurons might have long dendrites that extend into the external nuclear layer where spinal and trigeminal afferents terminate (Blomqvist et al., 1989;Saper, 1995). There is ultrastructural evidence that spinal and trigeminal afferents contact amygdala projection neurons in the lateral parabrachial area (Ma and Peschanski, 1988), but in this study, neither the laminae of origin of the spinal and trigeminal neur...

show abstract

Quantitative analysis of central terminal projections of visceral and somatic unmyelinated (C) primary afferent fibers in the guinea pig

Cited by 57 publications

References 80 publications

Central projection of unmyelinated (C) primary afferent fibers from gastrocnemius muscle in the guinea pig

Central projection of unmyelinated (C) primary afferent fibers from gastrocnemius muscle in the guinea pig

Primary Afferent Stimulation Differentially Potentiates Excitatory and Inhibitory Inputs to Spinal Lamina II Outer and Inner Neurons

Transneuronal Labeling of a Nociceptive Pathway, the Spino-(Trigemino-)Parabrachio-Amygdaloid, in the Rat

Contact Info

Product

Resources

About