Activation of the spinal neuronal network responsible for visceral control during locomotion

Merkulyeva, Natalia; Lyakhovetskii, Vsevolod; Veshchitskii, Aleksandr; Bazhenova, Elena; Gorskii, Oleg; Musienko, Pavel

doi:10.1016/j.expneurol.2019.112986

Cited by 10 publications

(13 citation statements)

References 56 publications

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“…The circuit functions of the remaining unidentified classes of ChAT − /TH − SPN neurons activated by cystometry is mostly unknown, but there is recent evidence suggesting that some may coordinate LUT functions with somatic activity (Thor & de Groat, 2010). This is consistent with activation of the SPN detected by c‐Fos mapping following locomotion in decerebrate cats (Merkulyeva et al, 2019). Coordination of LUT and hindlimb motor activities was demonstrated by correlations in EMGs recorded in bladder detrusor, external urinary sphincter, and hindlimb muscles.…”

Section: Discussionsupporting

confidence: 88%

Sex differences in c‐Fos and EGR‐1/Zif268 activity maps of rat sacral spinal cord following cystometry‐induced micturition

Wiedmann

Wong

Keast

et al. 2020

J of Comparative Neurology

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Storage and voiding of urine from the lower urinary tract (LUT) must be timed precisely to occur in appropriate behavioral contexts. A major part of the CNS circuit that coordinates this activity is found in the lumbosacral spinal cord. Immediate early gene (IEG) activity mapping has been widely used to investigate the lumbosacral LUT-related circuit, but most reports focus on the effects of noxious stimulation in anesthetized female rats. Here we use c-Fos and EGR-1 (Zif268) activity mapping of lumbosacral spinal cord to investigate cystometry-induced micturition in awake female and male rats. In females, after cystometry c-Fos neurons in spinal cord segments L5-S2 were concentrated in the sacral parasympathetic nucleus (SPN), dorsal horn laminae II-IV, and dorsal commissural nucleus (SDCom). Comparisons of cystometry and control groups in male and female revealed sex differences. Activity mapping suggested dorsal horn laminae II-IV was activated in females but showed net inhibition in males. However, inhibition in male rats was not detected by EGR-1 activity mapping, which showed low coexpression with c-Fos. A class of catecholamine neurons in SPN and SDCom neurons were also more strongly activated by micturition in females. In both sexes, most c-Fos neurons were identified as excitatory by their absence of Pax2 expression. In conclusion, IEG mapping in awake male and female rats has extended our understanding of the functional molecular anatomy of the LUT-related circuit in spinal cord. Using this approach, we have identified sex differences that were not detected by previous studies in anesthetized rats.

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Section: Discussionsupporting

confidence: 88%

Sex differences in c‐Fos and EGR‐1/Zif268 activity maps of rat sacral spinal cord following cystometry‐induced micturition

Wiedmann

Wong

Keast

et al. 2020

J of Comparative Neurology

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“…Although further investigation of the EES effects on the urodynamic activity of the Detr and EUS is required, this may be a promising tool for the treatment of LUT disturbances manifesting as an inability to store and expel urine. Besides the short-latency reflex response, we have also observed polysynaptic activity recruited by EES in Detr and EUS that is apparently due to activation of visceral and sensorimotor neuronal pathways underlying somatovisceral integrative mechanisms (Merkulyeva et al, 2019 ). Such mechanisms can be essential for the motor and autonomic functions recovery after SCI.…”

Section: Discussionmentioning

confidence: 67%

“…Most fibers of these roots carry sensorimotor information and form the peripheral nerves of the hind limbs. EUS activation during sacral stimulation can be associated with the somatovisceral integrative mechanisms (Merkulyeva et al, 2019 ). This effect is similar to tibial nerve stimulation, which is known to be effective in the clinical practice for EUS activation and treatment of the overactive bladder syndrome (Peters et al, 2010 , 2013 ).…”

Section: Discussionmentioning

confidence: 99%

“…Then the notch of insulation of 0.5 mm length was removed on each wire and the wires were sutured to the dura mater rostral and caudal to the exposed sites using 8.0 Ethilon suture. Then a midline lower abdominal incision was made to expose the bladder to implant the bladder catheter and stainless steel wire electrodes (AM-Systems, LLC, #793500) into the Detr, EUS (Scheepe et al, 1998 ; Merkulyeva et al, 2019 ). For surgical manipulations, the bladder was pulled out of the abdominal cavity, the access to the EUS was provided using a surgical dilator.…”

Section: Methodsmentioning

confidence: 99%

“…The EMG signals were differentially amplified (A-M Systems USA, model 1700, the bandwidth of 10 Hz–5 kHz) and digitized at 20 kHz with a National Instrument A/D board. The reflex responses to spinal cord stimulation were recorded from Detr (Craggs and Stephenson, 1976 ; Fry et al, 1998 ) and EUS (Merkulyeva et al, 2019 ) while the tested awake rat was sitting in the plastic box. Also, we recorded GM and TA EMG activity to control the triggering capacity of EES and specificity of this method in recruiting spinal reflex pathways (Gerasimenko et al, 2006 ).…”

Section: Methodsmentioning

confidence: 99%

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Site-Specific Neuromodulation of Detrusor and External Urethral Sphincter by Epidural Spinal Cord Stimulation

Sysoev

Bazhenova

Lyakhovetskii

et al. 2020

Front. Syst. Neurosci.

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Impairments of the lower urinary tract function including urine storage and voiding are widely spread among patients with spinal cord injuries. The management of such patients includes bladder catheterization, surgical and pharmacological approaches, which reduce the morbidity from urinary tract-related complications. However, to date, there is no effective treatment of neurogenic bladder and restoration of urinary function. In the present study, we examined neuromodulation of detrusor (Detr) and external urethral sphincter by epidural electrical stimulation (EES) of lumbar and sacral regions of the spinal cord in chronic rats. To our knowledge, it is the first chronic study where detrusor and external urethral sphincter signals were recorded simultaneously to monitor their neuromodulation by site-specific spinal cord stimulation (SCS). The data obtained demonstrate that activation of detrusor muscle mainly occurs during the stimulation of the upper lumbar (L1) and lower lumbar (L5-L6) spinal segments whereas external urethral sphincter was activated predominantly by sacral stimulation. These findings can be used for the development of neurorehabilitation strategies based on spinal cord epidural stimulation for autonomic function recovery after severe spinal cord injury (SCI).

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Postnatal growth of the lumbosacral spinal segments in cat: Their lengths and positions in relation to vertebrae

Shkorbatova

Lyakhovetskii

Veshchitskii

et al. 2022

The Anatomical Record

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Cat is a prominent model for investigating neural networks of the lumbosacral spinal cord that control locomotor and visceral activity. We previously proposed an integral function, establishing the topographical relationship between the spinal cord segments and vertebrae in adult animals. Here, we investigated the dynamic of this topographical relationship through early and middle periods of development in kittens. We calculated the length of each vertebra relative to the total length of the region from 13th thoracic (T) to the 7th lumbar (L) vertebrae (V) as well as the length of each segment relative to the total region from T13 to the three-dimensional sacral (S) segment. As in our previous work, the length and position of VL2 were used to establish relationships between the characteristics of the segments and vertebrae. Cubic regression reliably approximates the lengths of segments relative to VL2 length. As the cat aged, the relative length of VT13 and VL1 decreased while the relative length of VL5 increased. The relative length of the T13 and L3 segments increased while the relative length of the S1-S2 segments decreased. The T13-L2 segments are descended monotonically relative to the VL1-VL2 border.The L3-S1 segments are also descended, though with more complex dynamics.The positions of the S2-S3 segments remained unchanged. To conclude, different spinal segments displayed different developmental dynamics. The revealed relationship between vertebrae and lumbosacral spinal segments may be helpful for clearly defining stimulation regions to invoke particular functions, both in experimental studies on the spinal cord and clinical treatment.

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Activation of the spinal neuronal network responsible for visceral control during locomotion

Cited by 10 publications

References 56 publications

Sex differences in c‐Fos and EGR‐1/Zif268 activity maps of rat sacral spinal cord following cystometry‐induced micturition

Sex differences in c‐Fos and EGR‐1/Zif268 activity maps of rat sacral spinal cord following cystometry‐induced micturition

Site-Specific Neuromodulation of Detrusor and External Urethral Sphincter by Epidural Spinal Cord Stimulation

Postnatal growth of the lumbosacral spinal segments in cat: Their lengths and positions in relation to vertebrae

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