Abstract
Variation in an animal's spatial environment can induce variation in the hippocampus, an area of the brain involved in spatial cognitive processing. Specifically, increased spatial area use is correlated with increased hippocampal attributes, such as volume and neurogenesis. In the side-blotched lizard (Uta stansburiana), males demonstrate alternative reproductive tactics and are either territorial—defending large, clearly defined spatial boundaries—or non-territorial—traversing home ranges that are smaller than the territorial males' territories. Our previous work demonstrated cortical volume (reptilian hippocampal homolog) correlates with these spatial niches. We found that territorial holders have larger medial cortices than non-territory holders, yet these differences in the neural architecture demonstrated some degree of plasticity as well. Although we have demonstrated a link among territoriality, spatial use, and brain plasticity, the mechanisms that underlie this relationship are unclear. Previous studies found that higher testosterone levels can induce increased use of the spatial area and can cause an upregulation in hippocampal attributes. Thus, testosterone may be the mechanistic link between spatial area use and the brain. What remains unclear, however, is if testosterone can affect the cortices independent of spatial experiences and whether testosterone differentially interacts with territorial status to produce the resultant cortical phenotype. In this study, we compared neurogenesis as measured by the total number of doublecortin-positive cells and cortical volume between territorial and non-territorial males supplemented with testosterone. We found no significant differences in the number of doublecortin-positive cells or cortical volume among control territorial, control non-territorial, and testosterone-supplemented non-territorial males, while testosterone-supplemented territorial males had smaller medial cortices containing fewer doublecortin-positive cells. These results demonstrate that testosterone can modulate medial cortical attributes outside of differential spatial processing experiences but that territorial males appear to be more sensitive to alterations in testosterone levels compared with non-territorial males.
Highlights
Animals that defend clearly delineated territories are in part reliant upon spatial memory to remember territorial boundaries and determine the location of territorial neighbors (Falls, 1982; Godard, 1991; McGregor and Westby, 1992; Sherry, 1998; Bee and Gerhardt, 2001)
Territorial behavior and territory size have been linked to testosterone, in that increased levels of testosterone correlate with increased territory size and improve spatial cognition in mammals, birds, and lizards (e.g., Wingfield, 1984; DeNardo and Sinervo, 1994; Moss et al, 1994; Sinervo et al, 2000; Veiga et al, 2001; Ketterson et al, 1996; Spritzer et al, 2011)
When controlling for remainder of the telencephalon volume, we found that dorsal cortical volume was not significantly affected by the covariate [F(1, 13) = 0.573, p = 0.462], territorial status [F(1, 13) = 0.015, p = 0.904], treatment [F(1, 13) = 0.022, p = 0.886], or the interaction [F(1, 13) = 134, p = 0.720]; analyses without the covariate yielded similar results [territorial status: F(1, 16) = 0.484, p = 0.497; treatment: F(1, 16) = 0.002, p = 0.963; interaction: F(1, 16) = 0.627, p = 0.440]
Summary
Animals that defend clearly delineated territories are in part reliant upon spatial memory to remember territorial boundaries and determine the location of territorial neighbors (Falls, 1982; Godard, 1991; McGregor and Westby, 1992; Sherry, 1998; Bee and Gerhardt, 2001). Previous studies in a variety of taxa have demonstrated that individuals that hold territories, hold larger territories, or traverse larger home ranges have better spatial memory These individuals have larger hippocampi, the area of the brain largely responsible for spatial memory processing, with more new hippocampal neurons, presumably to subserve the increased demands on spatial cognition (Gaulin and Fitzgerald, 1986, 1989; Jacobs et al, 1990; Galea and McEwen, 1999; Amrein et al, 2004; Roth et al, 2006; LaDage et al, 2009, 2013; Holding et al, 2012). While testosterone has been linked to both territoriality and hippocampal attributes, it remains unclear if testosterone is the underlying mechanism that links the two and, if so, whether variation in testosterone can directly alter brain attributes, outside of spatial area use experiences
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