Functional Connectivity among Limbic Brain Areas: Differential Effects of Incubation Temperature and Gonadal Sex in the Leopard Gecko, <i>Eublepharis macularius</i>

Abstract

The neural basis of individual differences in behavior has been studied primarily by analyzing the properties of specific neural areas. However, because of the organization of the nervous system, it is also plausible that differences in behavior are mediated by differences in the interactivity or functional connectivity among brain nuclei in particular neural circuits. In the leopard gecko, Eublepharis macularius, the temperature of the egg during incubation not only determines gonadal sex, but also shapes the sociosexual behaviors, reproductive physiology, and hormone sensitivity of adult animals. In this study the effects of both incubation temperature and gonadal sex on functional connectivity among limbic brain areas were examined. Functional connectivity was assessed by analyzing covariance patterns in metabolic capacity, as revealed by quantitative cytochrome oxidase histochemistry. It was hypothesized that incubation temperature and gonadal sex affect the propensity to display aggressive or sexual behaviors by altering the functional connectivity within relevant neural circuits. The correlations of metabolic capacity between the anterior hypothalamus and both the septum and preoptic area were significant only in relatively aggressive individuals, suggesting that these circuits may regulate the phenotypic variation in aggressiveness caused by incubation temperature. The correlations between the ventromedial hypothalamus and both the dorsal ventricular ridge and septum were significant only in females, suggesting that these circuits may modulate female-typical sexual behaviors. Correlations among preoptic, hypothalamic and amygdalar areas tended to be distributed across both sexes, suggesting that there may be shared pathways underlying the expression of male-typical and female-typical behaviors.

The vertebrate social behavior network: Evolutionary themes and variations

“…While most relevant findings have come from birds, consistent data are also available for amphibians, fish and reptiles (see Table 1 and the following two sections), and Newman's model has been explicitly applied as a conceptual framework for data in geckos (Eublepharis macularius) (Crews, 2003). Interestingly, data from geckos demonstrate that behavioral variations are correlated with distinct patterns of functional connectivity within the network (Sakata et al, 2000;Sakata and Crews, 2004), a finding that lends good empirical support to Newman's (1999) ideas about the significance of distributed activation patterns.…”

“…While most relevant findings have come from birds, consistent data are also available for amphibians, fish and reptiles (see Table 1 and the following two sections), and Newman's model has been explicitly applied as a conceptual framework for data in geckos (Eublepharis macularius) (Crews, 2003). Interestingly, data from geckos demonstrate that behavioral variations are correlated with distinct patterns of functional connectivity within the network (Sakata et al, 2000;Sakata and Crews, 2004), a finding that lends good empirical support to Newman's (1999) ideas about the significance of distributed activation patterns.Our own research expands upon these studies in two important respects: First, our work on the vocal circuitry of the plainfin midshipman fish (Porichthys notatus) provides the first comprehensive mapping of the network's connections in a non-mammal, and has yielded strong evidence that the social behavior network arose in the earliest vertebrates (Goodson and Bass, 2002). As detailed below, the vocal system of the midshipman offers opportunities for systemslevel experiments on the network that are not possible in most other animals (i.e., the whole brain can be exposed during analyses of social behavior patterning); thus understanding the comparative organization of the relevant circuitry in fish is particularly valuable.…”

Functional networks underlying latent inhibition learning in the mouse brain

“…Schmajuk et al (1996); et al, 2000). Differences in mean CO activity reflect differences in the metabolic capacity of particular brain areas, whereas differences in correlations in CO activity between regions reflect differences in functional coupling among brain areas (Sakata et al 2000). Consequently, CO can be used to determine functional pathways modified as a consequence of learning.…”

“…A complementary approach is to investigate the interactions between brain regions. This approach is based on the finding that brain regions that are functionally coupled show coordinated changes in metabolic capacity, which is manifested in the strength of the correlation of CO activity between regions (Sakata et al, 2000). Differences in mean CO activity reflect differences in the metabolic capacity of particular brain areas, whereas differences in correlations in CO activity between regions reflect differences in functional coupling among brain areas (Sakata et al 2000).…”

Enhanced metabolic capacity of the frontal cerebral cortex after Pavlovian conditioning

“…Cytochrome oxidase (CO) metabolic brain mapping provides an alternative approach for investigating neural circuits mediating Pavlovian conditioning, and it is a well-suited method for quantifying more stable neuronal metabolic capacity changes that reflect prolonged training (Poremba et al, 1997, Poremba et al, 1998b, Poremba et al, 1998a, Sakata et al, 2000, Villarreal et al, 2002, Conejo et al, 2005, Sakata et al, 2005. CO changes in the brain after prolonged training reach a more stabilized state of oxidative metabolism, and techniques which measure evoked brain metabolic activity, such as fluorodeoxyglucose (FDG) autoradiography, positron emission tomography (PET) or functional magnetic resonance imaging (fMRI) may not reflect sustained changes in baseline metabolic capacity (Gonzalez-Lima and Cada, 1998).…”