Obesity-inducing amygdala lesions: examination of anterograde degeneration and retrograde transport

Abstract

King, Bruce M., Jack T. Cook, Kirk N. Rossiter, and Bethany L. Rollins. Obesity-inducing amygdala lesions: examination of anterograde degeneration and retrograde transport. Am J Physiol Regul Integr Comp Physiol 284: R965-R982, 2003. First published November 14, 2002 10.1152/ajpregu.00249.2002.-Small lesions centered in the posterodorsal region of the medial amygdala resulted in excessive weight gains in female rats. Unilateral lesions were nearly as effective as bilateral lesions in the first 48 h after surgery (ϩ21 to ϩ32 g). Assessment of lesion damage was done by both qualitative evaluation and by a quantitative grid-point counting method. The critical sites for weight gain were the intra-amygdaloid bed nucleus of the stria terminalis and the posterodorsal medial amygdaloid nucleus. Incidental damage to the overlying globus pallidus was negatively related to weight gain. The cupric silver method for demonstrating axonal degeneration was applied to brains with obesity-inducing lesions. A dense pattern of degenerating terminals was found in the lateral septum, amygdala, ventral striatum, and ventromedial hypothalamus. Degeneration in the paraventricular nucleus of the hypothalamus was scarce or absent. Small retrograde tracer injections made in either the intra-amygdaloid bed nucleus of the stria terminalis or in the posterodorsal medial amygdaloid nucleus labeled cells in the amygdala, lateral septum, and hypothalamus, reciprocating the anterograde projections from the amygdala to these areas. The data suggest that subdivisions of the posterodorsal amygdala participate in the regulation of feeding in a manner that is similar to the better-known role of this part of the brain in mediating reproductive behavior. Although topographical differences may exist within the amygdaloid and hypothalamic subdivisions regulating these two sexually dimorphic behaviors, the relays engaged by feeding-related connections and those related to reproduction are remarkably parallel. nucleus accumbens; hypothalamus; stria terminalis SEVERAL RECENT STUDIES have demonstrated that bilateral electrolytic lesions of the amygdala in female rats can result in marked hyperphagia and excessive weight gains. Daily food intake nearly doubles, and weight gains of 20-30 g during the first 3 days after lesions are not unusual (e.g., 45, 50-53, 84). Weight gains of Ն100 g in 20-25 days have been observed (50, 51). The lesions result in a marked preference for carbohydrates (53). Although food intake eventually returns to normal, the excessive weight gain is maintained indefinitely, with a marked increase in adipose tissue (50).These results are similar to those reported many years ago for cats, dogs, and primates (including humans) given amygdaloid lesions or temporal lobectomies (e.g., 9, 32, 37, 70, 103). In the rat, the effective lesion site for hyperphagia and obesity has recently been identified as the posterodorsal part of the medial amygdaloid nucleus (MePD) and the intra-amygdaloid bed nucleus of the stria terminalis (BSTIA), together ...

Glutamate Microinjected in the Posterodorsal Medial Amygdala Induces Subtle Increase in the Consumption of a Three‐Choice Macronutrient Self‐Selection Diet in Male Rats

“…As evidenced by electrophysiological recordings, not all hypothalamic neurons sampled responded to MeA stimulation but, when it occurred, both excitatory and inhibitory responses were evoked in different target areas (Carrer et al, 1978;Choi et al, 2005;Bian et al, 2008). It is also conceivable that lesions involving the ''posterodorsal amygdala'' and that induced hyperphagia (King et al, 1998(King et al, , 1999(King et al, , 2003Rollins and King, 2000;Grundmann et al, 2005) have affected other amygdaloid nuclei or transition areas besides the MePD (Rollins and King, 2000;King et al, 2003;Moscarello et al, 2009). In effect, excessive weight gains in lesioned females might be more related to damage the intra-amygdaloid division of the bed nucleus of the ST than to the MePD itself (King et al, 1998).…”

“…Previous reports involved the ''posterodorsal region'' of the amygdala with feeding behavior in rats (King et al, 1998(King et al, , 1999(King et al, , 2003Rollins and King, 2000;Grundmann et al, 2005). This wide area is neither an anatomical nor a functional unit; rather, it involves different amygdaloid components, such as the medial nucleus of the amygdala (MeA), the stria terminalis (ST), and the bed nucleus of the ST among others.…”

“…This wide area is neither an anatomical nor a functional unit; rather, it involves different amygdaloid components, such as the medial nucleus of the amygdala (MeA), the stria terminalis (ST), and the bed nucleus of the ST among others. Unilateral or bilateral electrolytic lesions of this ''posterodorsal region'' led Long-Evans adult female rats to display a marked preference for carbohydrate consumption, hyperphagia, and an abnormal increase in body weight (King et al, 1998(King et al, , 1999(King et al, , 2003. Lesions also promoted anterograde degeneration in the ipsilateral hypothalamic ventromedial nucleus (Rollins and King, 2000;Grundmann et al, 2005), an integrated area for the central control of food intake and energy balance (Berthoud, 2002).…”

Approaching the shared biology of obesity and depression: the stress axis as the locus of gene–environment interactions

“…103 Critical sites for weight gain are located in the amygdala; minor lesions centered on the posterodorsal region of the medial amygdala result in excessive weight gains in rats. 104 Functional magnetic resonance scanning has shown increased activation of visual food stimuli in the amygdala 105 in obese individuals.…”

Genes involved in obesity: Adipocytes, brain and microflora

“…In fact, intra-PVN injection of NPY increases food intake, more specifically carbohydrate intake (Stanley et al, 1985). Arcuate NPY neurons also send innervation to amygdala, an area also involved in feeding behaviour since lesion of amygdala produces obesity and increases preference for high carbohydrate diet (King et al, 1998;King et al, 2003). When administrated into the amygdala, NPY selectively reduces high fat food intake and preference, without altering total caloric intake (Primeaux et al, 2006).…”