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PERSPECTIVES |
1 Neuroscience Pennington Biomedical Research Center-LSU System, 6400 Perkins, Road, Baton Rouge, LA, 70808, USA
Email: alberto.travagli{at}pbrc.edu
Over the years many of our neuroscience colleagues have questioned our reasons for studying ‘boring’ brainstem autonomic circuits. Their assumption was that the neurons comprising these reflex pathways were simply relay stations with no ‘personality’, i.e. the response of the neuronal population ‘in toto’ was already pre-determined resulting in a generic, stereotyped and predictable outcome. All integrative capabilities for modulation of cardiorespiratory or gastrointestinal reflexive functions were to be determined by ‘higher’ neuronal systems such as the hypothalamus or the enteric nervous system. An increasingly large amount of evidence confuting this diminutive concept of brainstem reflexive circuits, though, is starting to emerge.
Neurons of the nucleus tractus solitarius (NTS) receive vagal sensory information from cardiorespiratory and subdiaphragmatic organs of the gastrointestinal tract. NTS neurons comprise many intermixed cellular types encompassing a vast array of neurochemical phenotypes scattered throughout the various NTS subnuclei with no apparent organization. This type of apparent dissociated organization makes it hard to identify with certainty the visceral inputs and function(s) of specific neuronal populations and only an approximate guess can be made with regards to their target organ.
In this issue of The Journal of Physiology, Bailey and colleagues (Bailey et al. 2007) combine neuroanatomical tracing techniques with an electrophysiological approach in horizontal brainstem slice preparations to identify and characterize NTS neurons that project selectively to either the paraventricular nucleus of the hypothalamus (PVN) or the caudal ventrolateral medulla (CVLM). This experimental strategy allows the correlation between long distance connections (PVN and CVLM) and the ‘black box’ of the local networks of the NTS. In their work, Bailey and colleagues report that identified NTS neurons projecting to PVN can be distinguished from those neurons projecting to CVLM based on the presence of the fast-transient IA-like potassium current, on their larger soma size and their more complex dendritic morphology. Conversely, CVLM-projecting NTS neurons had a more faithful response to stimulation of the tractus solitarius. The paper by Bailey et al. is just the most recent work in a series of publications from this group that aim to provide evidence of the exquisite organization of these pathways and networks in the control of cardiovascular functions (Bailey et al. 2002; Jin et al. 2004). Our group is conducting research with a very similar focus, although concentrating on the circuits controlling gastrointestinal homeostatic functions (Browning et al. 2006; Browning & Travagli, 2006). The overall idea driving the work of these groups is that brainstem circuits are specialized or tuned at multiple levels, starting from the neuronal membrane itself and working up from the local network connections to the pathways projecting to very distant areas. The biophysical, pharmacological and synaptic diversity in the neuronal organization, although confusing (we are just at the beginning of the discovery phase), may actually represent meaningful patterns of specialization or segregated lines of specificity, where synaptic inputs and membrane characteristics offer a level of potential mechanistic redundancy that allows adjacent neurons to ‘recognize’ and reinforce each other's common pathway and goal.
This type of cellular organization implies a ‘task matching’ capability even within the brainstem neurons of the NTS. In fact, although small in size, the NTS is devoted to the integration of vital cardiac, respiratory and gastrointestinal functions, whose demands vary greatly both in terms of timing as well as duration of response. Whilst we can afford to have a gastrointestinal response occurring with a delay of a few seconds (or minutes), such an untimely response would certainly be incompatible with life when applied to the control of the baroreflex or respiration.
This type of cellular organization within the NTS should force us to be extremely cautious in the physiological interpretation of generic manipulations that analyse a single outcome such as cFos expression, calcium oscillations, blood pressure or gastric motility responses to microinjections. A multifaceted approach that includes the electrophysiological analysis of cellular mechanisms is needed to put in place the pieces of the puzzle of that beautiful ‘task-matching’ black box of the NTS.
References
Bailey TW, Hermes SM, Whittier KL, Aicher SA & Andresen MC (2007). J Physiol 582, 613–628.
Bailey TW, Jin YH, Doyle MW & Andresen MC (2002). J Neurosci 22, 8230–8237.
Browning KN & Travagli RA (2006). Auton Neurosci 126–127, 2–8.
Browning KN, Zheng Z, Gettys TW & Travagli RA (2006). J Physiol 575, 761–776.
Jin YH, Bailey TW, Li BY, Schild JH & Andresen MC (2004). J Neurosci 24, 4709–4717.
Related Article
J. Physiol. 2007 582: 613-628.
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