Article

Energetic responses to cold temperatures in rats lacking forebrain-caudal brain stem connections

Graduate Groups of Psychology and Neuroscience, Univ. of Pennsylvania, 3720 Walnut St., Philadelphia, PA 19104, USA.
AJP Regulatory Integrative and Comparative Physiology (Impact Factor: 3.11). 09/2008; 295(3):R789-98. DOI: 10.1152/ajpregu.90394.2008
Source: PubMed

ABSTRACT

Hypothalamic neurons are regarded as essential for integrating thermal afferent information from skin and core and issuing commands to autonomic and behavioral effectors that maintain core temperature (T(c)) during cold exposure and for the control of energy expenditure more generally. Caudal brain stem neurons are necessary elements of the hypothalamic effector pathway and also are directly driven by skin and brain cooling. To assess whether caudal brain stem processing of thermal afferent signals is sufficient to drive endemic effectors for thermogenesis, heart rate (HR), T(c), and activity responses of chronic decerebrate (CD) and control rats adapted to 23 degrees C were compared during cold exposure (4, 8, or 12 degrees C) for 6 h. Other CDs and controls were exposed to 4 or 23 degrees C for 2 h, and tissues were processed for norepinephrine turnover (NETO), a neurochemical measure of sympathetic drive. Controls maintained T(c) for all temperatures. CDs maintained T(c) for the 8 and 12 degrees C exposures, but T(c) declined 2 degrees C during the 4 degrees C exposure. Cold exposure elevated HR in CDs and controls alike. Tachycardia magnitude correlated with decreases in environmental temperature for controls, but not CDs. Cold increased NETO in brown adipose tissue, heart, and some white adipose tissue pads in CDs and controls compared with their respective room temperature controls. These data demonstrate that, in neural isolation from the hypothalamus, cold exposure drives caudal brain stem neuronal activity and engages local effectors that trigger sympathetic energetic and cardiac responses that are comparable in many, but not in all, respects to those seen in neurologically intact rats.

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    • "Therefore, only NETO should be measured in AMPT-treated animals with a parallel set of animals used for non-NETO measures. With this method we (Brito et al., 2007, 2008; Mul et al., 2013; Nautiyal et al., 2008; Shi et al., 2004; Youngstrom and Bartness, 1995) and others (Garofalo et al., 1996; Harris, 2012; Lazzarini and Wade, 1991; Migliorini et al., 1997; Penn et al., 2006) have measured differential NETO across WAT depots and BAT showing the fat pad-specific patterns of sympathetic drive that are triggered by various energy demanding challenges. Thus, for measures of SNS drive in non-human animals we see the AMPT method as preferable to electrophysiological measures because with the latter usually only innervation to one or two tissues can be measured at a time because of electrical interference, whereas with the AMPT method the number of tissues that can be simultaneously assayed are only limited by one's interest. "
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    ABSTRACT: White adipose tissue (WAT) is innervated by the sympathetic nervous system (SNS) and its activation is necessary for lipolysis. WAT parasympathetic innervation is not supported. Fully-executed SNS-norepinephrine (NE)-mediated WAT lipolysis is dependent on β-adrenoceptor stimulation ultimately hinging on hormone sensitive lipase and perilipin A phosphorylation. WAT sympathetic drive is appropriately measured by electrophysiological and neurochemical (NE turnover) in non-human animals and this drive is fat pad-specific preventing generalizations among WAT depots and non-WAT organs. Leptin-triggered SNS-mediated lipolysis is weakly supported, whereas insulin or adenosine inhibition of SNS/NE-mediated lipolysis is strongly supported. In addition to lipolysis control, increases or decreases in WAT SNS drive/NE inhibit and stimulate white adipocyte proliferation, respectively. WAT sensory nerves are of spinal-origin and sensitive to local leptin and increases in sympathetic drive, the latter implicating lipolysis. Transsynaptic viral tract tracer use revealed WAT central sympathetic and sensory circuits including SNS-sensory feedback loops that may control lipolysis.
    Full-text · Article · Apr 2014 · Frontiers in Neuroendocrinology
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    • "Therefore, only NETO should be measured in AMPT-treated animals with a parallel set of animals used for non-NETO measures. With this method we (Brito et al., 2007, 2008; Mul et al., 2013; Nautiyal et al., 2008; Shi et al., 2004; Youngstrom and Bartness, 1995) and others (Garofalo et al., 1996; Harris, 2012; Lazzarini and Wade, 1991; Migliorini et al., 1997; Penn et al., 2006) have measured differential NETO across WAT depots and BAT showing the fat pad-specific patterns of sympathetic drive that are triggered by various energy demanding challenges. Thus, for measures of SNS drive in non-human animals we see the AMPT method as preferable to electrophysiological measures because with the latter usually only innervation to one or two tissues can be measured at a time because of electrical interference, whereas with the AMPT method the number of tissues that can be simultaneously assayed are only limited by one's interest. "
    [Show abstract] [Hide abstract]
    ABSTRACT: White adipose tissue (WAT) is innervated by the sympathetic nervous system (SNS) and its activation is necessary for lipolysis. WAT parasympathetic innervation is not supported. Fully-executed SNS-norepinephrine (NE)-mediated WAT lipolysis is dependent on β-adrenoceptor stimulation ultimately hinging on hormone sensitive lipase and perilipin A phosphorylation. WAT sympathetic drive is appropriately measured by electrophysiological and neurochemical (NE turnover) in non-human animals and this drive is fat pad-specific preventing generalizations among WAT depots and non-WAT organs. Leptin-triggered SNS-mediated lipolysis is weakly supported, whereas insulin or adenosine inhibition of SNS/NE-mediated lipolysis is strongly supported. In addition to lipolysis control, increases or decreases in WAT SNS drive/NE inhibit and stimulate white adipocyte proliferation, respectively. WAT sensory nerves are of spinal-origin and sensitive to local leptin and increases in sympathetic drive, the latter implicating lipolysis. Transsynaptic viral tract tracer use revealed WAT central sympathetic and sensory circuits including SNS-sensory feedback loops that may control lipolysis.
    Full-text · Article · Jan 2014 · Frontiers in Neuroendocrinology
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    • "Rats maintained with a brainstem transection just rostral to the superior colliculus (Nautiyal et al., 2008) or with bilateral cuts just caudal to the POA (Blatteis and Banet, 1986) can mount relatively normal cold-defense responses, leading to the conclusion that the POA is not essential for the integration of autonomic thermoregulatory responses in the rat and that circuits caudal to the transection are sufficient to convey cutaneous thermal information to the premotor neurons in the rRPa necessary to evoke cold-defense responses. Why the pathways proposed by these investigators to explain these effects in transected rats are ineffective in intact rats following neuronal inhibition of hypothalamic sites in intact animals (Zaretskaia et al., 2003; Madden and Morrison, 2004; Nakamura and Morrison, 2007, 2008a) remains unexplained. "
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    ABSTRACT: Thermogenesis, the production of heat energy, is an essential component of the homeostatic repertoire to maintain body temperature during the challenge of low environmental temperature and plays a key role in elevating body temperature during the febrile response to infection. Mitochondrial oxidation in brown adipose tissue (BAT) is a significant source of neurally regulated metabolic heat production in many species from mouse to man. BAT thermogenesis is regulated by neural networks in the central nervous system which responds to feedforward afferent signals from cutaneous and core body thermoreceptors and to feedback signals from brain thermosensitive neurons to activate BAT sympathetic nerve activity. This review summarizes the research leading to a model of the feedforward reflex pathway through which environmental cold stimulates BAT thermogenesis and includes the influence on this thermoregulatory network of the pyrogenic mediator, prostaglandin E(2), to increase body temperature during fever. The cold thermal afferent circuit from cutaneous thermal receptors, through second-order thermosensory neurons in the dorsal horn of the spinal cord ascends to activate neurons in the lateral parabrachial nucleus which drive GABAergic interneurons in the preoptic area (POA) to inhibit warm-sensitive, inhibitory output neurons of the POA. The resulting disinhibition of BAT thermogenesis-promoting neurons in the dorsomedial hypothalamus activates BAT sympathetic premotor neurons in the rostral ventromedial medulla, including the rostral raphe pallidus, which provide excitatory, and possibly disinhibitory, inputs to spinal sympathetic circuits to drive BAT thermogenesis. Other recently recognized central sites influencing BAT thermogenesis and energy expenditure are also described.
    Full-text · Article · Jan 2012 · Frontiers in Endocrinology
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