A comparative reappraisal of projections from the superficial laminae of the dorsal horn in the rat: The forebrain

Gauriau, Caroline; Bernard, Jean‐François

doi:10.1002/cne.10873

Cited by 183 publications

(164 citation statements)

References 144 publications

(243 reference statements)

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“…LSN neurons project bilaterally to the mediodorsal thalamic nucleus and some authors assume that this LSN-mediodorsal pathway may be involved in the emotional and cognitive aspects of pain (Gauriau and Bernard, 2004).…”

Section: Axon Architecture Of Neurons Outside the Superficial Dorsal mentioning

confidence: 99%

“…In case of the four bilateral projection neurons in our sample the splitting of the main axon occurs earlier and the two equally strong branches seemingly ascend in different tracts from the beginning. Since LSN is known to project bilaterally to the mediodorsal thalamic nucleus (Gauriau and Bernard 2004), it would be tempting to say that bilaterally projecting neurons may contribute to this double projection. However, from a metabolic point of view, bilateral projection this way would be very inefficient due to the high energy cost of maintaining the two branches.…”

Section: Bilaterally Projecting Axonsmentioning

confidence: 99%

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Neurons in the lateral part of the lumbar spinal cord show distinct novel axon trajectories and are excited by short propriospinal ascending inputs

et al. 2015

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Order of Authors Secondary Information:The role of spinal dorsal horn propriospinal connections in nociceptive processing is not yet established. Recently described, rostrocaudally oriented axon collaterals of lamina I projection and local-circuit neurons (PNs and LCNs) running in the dorsolateral funiculus (DLF) may serve as the anatomical substrate for intersegmental processing. Putative targets of these axons include lateral dendrites of superficial dorsal horn neurons, including PNs, and also neurons in the lateral spinal nucleus (LSN) that are thought to be important integrator units receiving, among others, visceral sensory information. Here we used an intact spinal cord preparation to study intersegmental connections within the lateral part of the superficial dorsal horn. We detected brief monosynaptic and prolonged polysynaptic excitation of lamina I and LSN neurons when stimulating individual dorsal horn neurons located caudally, even in neighbouring spinal cord segments. These connections, however, were infrequent. We also revealed that some projection neurons outside the dorsal grey matter and in the LSN have distinct, previously undescribed course of their projection axon. Our findings indicate that axon collaterals of lamina I PNs and LCNs in the DLF rarely form functional connections with other lamina I and LSN neurons and that the majority of their targets are on other elements of the dorsal horn. The unique axon trajectories of neurons in the dorsolateral aspect of the spinal cord, including the LSN do not fit our present understanding of midline axon guidance and suggest that their function and development differ from the neurons inside lamina I. These findings emphasize the importance of understanding the connectivity matrix of the superficial dorsal horn in order to decipher spinal sensory information processing. Powered by Editorial Manager® and ProduXion Manager® from Aries Systems Corporation Answers to Reviewer 1First of all, the authors would like to thank Reviewer 1 for his constructive comments and suggestions that helped us improving the manuscript. Below we give detailed answers to all major and minor concerns raised. Major issues 1)We completely agree with the reviewer that the statistical analysis would have helped to make our conclusions on morphometric parameters stronger. The reason why we decided to talk about the tendencies only without statistical tests was the low number of the reconstructed neurons in the groups. However, since we observed and wanted to demonstrate the difference between neurons within and outside lamina I (in the adjacent lateral white matter), in this revised version we pooled projection neurons (PNs) and localcircuit neurons (LCNs) from our previous reports to form a group of cells in lamina I called "L-I" whereas neurons lateral to the edge of the dorsal horn and in the LSN are now referred to as "OUT/LSN". Statistical analyses were performed between these two groups and showed significant differences in the morphometric parameters investigated, with the...

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Section: Axon Architecture Of Neurons Outside the Superficial Dorsal mentioning

confidence: 99%

Section: Bilaterally Projecting Axonsmentioning

confidence: 99%

Neurons in the lateral part of the lumbar spinal cord show distinct novel axon trajectories and are excited by short propriospinal ascending inputs

et al. 2015

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“…Within the framework of the somatosensory system, the spinothalamocortical pathway is wellknown to mediate perception and discrimination of cutaneous temperature sensation 9,10 and the signals are relayed by thalamic neurons in the VPM/VPL in rats 29,30 . In the present study, lesions of the VPM/VPL had no effect on skin cooling-evoked thermogenesis, but eliminated skin temperature-dependent changes in EEG recorded from the primary somatosensory cortex.…”

Section: Discussionmentioning

confidence: 99%

A thermosensory pathway that controls body temperature

2007

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Defending body temperature against environmental thermal challenges is one of the most fundamental homeostatic functions governed by the nervous system. Here we show a novel somatosensory pathway, which essentially constitutes the afferent arm of the thermoregulatory reflex triggered by cutaneous sensation of environmental temperature changes. Using rat in vivo electrophysiological and anatomical approaches, we revealed that lateral parabrachial neurons play a pivotal role in this pathway by glutamatergically transmitting cutaneous thermosensory signals received from spinal somatosensory neurons directly to the thermoregulatory command center, preoptic area. This feedforward pathway mediates not only sympathetic and shivering thermogenic responses but also metabolic and cardiac responses to skin cooling challenges. Notably, this 'thermoregulatory afferent' pathway exists in parallel with the spinothalamocortical somatosensory pathway mediating temperature perception. These findings make an important contribution to our understanding of both the somatosensory system and thermal homeostasis-two mechanisms fundamental to the nervous system and to our survival.Even during rapid changes in environmental temperature, the body temperature of homeothermic animals, including humans, is maintained within the narrow range necessary for optimal cellular and molecular functions. How the nervous system functions to defend body temperature against environmental thermal challenges remains a fundamental question in physiology 1,2 . The preoptic area (POA) is the thermoregulatory center providing command signals descending to peripheral effectors 1,3-6 . To evoke behavioral, autonomic, somatic and hormonal responses counteracting changes in environmental temperature before they impact body core temperature, thermoregulatory command neurons in the POA need to receive feedforward signaling of environmental temperature information from skin thermoreceptors through the spinal and trigeminal dorsal horns 3,5-8 . However, the neural substrate for the ascending thermoregulatory feedforward pathway, especially the essential central mechanism linking the second order somatosensory neurons in the dorsal horn to the POA has yet to be identified.The best-known central pathway for somatosensory signaling of cutaneous thermal sensation is the spinothalamocortical pathway, in which signals from skin thermoreceptors are transmitted through a direct projection from the dorsal horn to the thalamus and then relayed to the primary somatosensory cortex 9,10 . Although the spinothalamocortical pathway is responsible for perception and discrimination of cutaneous temperature 9,10 , it is unknown whether this pathway contributes to homeostatic responses against changes in environmental

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“…Nonetheless, this important link now gives rise to a strong controversy (Willis et al, 2002). Recently, we demonstrated in the rat that lamina I neurons, a major nociceptive relay of the dorsal horn, project densely not only to the ventrobasal complex but also on the posterior triangular (PoT) thalamic nucleus (Gauriau and Bernard, 2004). The PoT is a caudal extent of the thalamic posterior group (Po), located between the medial portion of the medial geniculate nucleus (MGM) and the anterior pretectal (APT) area (Paxinos and Watson, 1998).…”

Section: Introductionmentioning

confidence: 99%

“…The PoT projects at least in part, to the insular cortex . Taking together these points, we hypothesized that the PoT could convey nociceptive messages toward the insular cortex in the rat, as the VMpo does in the primate (Gauriau and Bernard, 2004).…”

Section: Introductionmentioning

confidence: 99%

Posterior Triangular Thalamic Neurons Convey Nociceptive Messages to the Secondary Somatosensory and Insular Cortices in the Rat

Gauriau

Bernard²

2004

J. Neurosci.

112

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This study investigated the responses of posterior triangular (PoT) thalamic neurons to tactile and noxious calibrated stimuli in anesthetized rats. We report here that 41% of PoT units responded to cutaneous stimulation, in most cases, by increasing strongly their firing. Forty-five percent of the responding units were nociceptive specific (NS), 19% were nociceptive nonspecific (NNS), and 36% were tactile. The NS units responded only to frankly noxious stimuli applied to relatively large receptive fields (several parts of the body). They encoded nociceptive temperatures chiefly in 46 -50°C ranges. The NNS units resembled NS units but also responded to innocuous stimuli. Tactile units responded chiefly to repeated innocuous stimuli applied to very small receptive fields (one to two fingers or vibrissae).A representative sample of PoT somatosensory neurons, characterized first by their response to innocuous and noxious cutaneous stimuli, were filled with juxtacellular injection of biotin-dextran that made it possible to label adequately the soma, the dendrites, and the entire axon of PoT neurons. We observed that the axons of NS neurons terminated only in secondary somatosensory (S2) cortex, whereas the axons of NNS and tactile neurons projected chiefly to the insular cortex and the amygdala.In conclusion, our results demonstrate a spinal-PoT-S2/insular cortices nociceptive pathway that conveys nociceptive messages arising from lamina I and spinal neurons of deep laminas. Furthermore, our results demonstrate for the first time that projections of PoT neurons are correlated to their physiological properties.

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A comparative reappraisal of projections from the superficial laminae of the dorsal horn in the rat: The forebrain

Cited by 183 publications

References 144 publications

Neurons in the lateral part of the lumbar spinal cord show distinct novel axon trajectories and are excited by short propriospinal ascending inputs

Neurons in the lateral part of the lumbar spinal cord show distinct novel axon trajectories and are excited by short propriospinal ascending inputs

A thermosensory pathway that controls body temperature

Posterior Triangular Thalamic Neurons Convey Nociceptive Messages to the Secondary Somatosensory and Insular Cortices in the Rat

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