Lateralization of the Vertebrate Brain: Taking the Side of Model Systems: Figure 1.

Halpern, Marnie E.; Güntürkün, Onur; Hopkins, William D.; Rogers, Lesley J.

doi:10.1523/jneurosci.3439-05.2005

Cited by 141 publications

(105 citation statements)

References 84 publications

(74 reference statements)

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“…Our study therefore indicates that the left NCM circuit is modulated by neuroestrogens to fine-tune song processing and preference. Circulating estrogens can asymmetrically influence human cortical activity over days to weeks (17,18), and the present results suggest that acute estrogen actions could be critical for lateralized sensory processing, a widespread feature of the vertebrate forebrain (19). Further, here local estrogen production directly influenced the encoding of species-specific song elements, revealing an exquisite specificity for acute neurosteroid modulation of complex sensory encoding.…”

Section: Discussionmentioning

confidence: 50%

Brain estrogens rapidly strengthen auditory encoding and guide song preference in a songbird

Remage‐Healey

Coleman

Oyama

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

191

224

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Higher cognitive function depends on accurate detection and processing of subtle features of sensory stimuli. Such precise computations require neural circuits to be modulated over rapid timescales, yet this modulation is poorly understood. Brainderived steroids (neurosteroids) can act as fast signaling molecules in the vertebrate central nervous system and could therefore modulate sensory processing and guide behavior, but there is no empirical evidence for this possibility. Here we report that acute inhibition of estrogen production within a cortical-like region involved in complex auditory processing disrupts a songbird's ability to behaviorally respond to song stimuli. Identical manipulation of local estrogen levels rapidly changes burst firing of single auditory neurons. This acute estrogen-mediated modulation targets song and not other auditory stimuli, possibly enabling discrimination among species-specific signals. Our results demonstrate a crucial role for neuroestrogen synthesis among vertebrates for enhanced sensory encoding. Cognitive impairments associated with estrogen depletion, including verbal memory loss in humans, may therefore stem from compromised moment-by-moment estrogen actions in higher-order cortical circuits.I n vertebrates, steroid hormones can rapidly influence the activity of neurons and neural circuits (1-3), although the functional consequences for higher processing are unclear. The exquisite recognition of species-typical vocalizations (4, 5) and abundant production of neuroestrogens (6, 7) are both especially prominent in songbirds. A cortical-like auditory region (the caudomedial nidopallium, or NCM) of songbirds is a critical locus for song learning as well as auditory processing and song recognition (8-11). NCM exhibits rich expression of the estrogen-synthetic enzyme aromatase in both cell bodies and synaptic terminals (6, 12), and neuroestrogen levels within NCM fluctuate rapidly (<30 min) and independent of peripheral sex-steroid levels during social interactions, song playback, and after neurotransmitter activation (13). In songbirds, therefore, rapid changes in the local production of NCM neuroestrogens could in turn rapidly affect processing of complex auditory stimuli, such as song.Here, we test this hypothesis in male Australian zebra finches (Taeniopygia guttata). Our recent optimization of in vivo microdialysis in this species has enabled the measurement and manipulation of local estrogen production within discrete brain regions in awake, behaving males (13). We have further established that local estrogen levels are dependent on the activity of the enzyme aromatase within NCM, because retrodialysis (reverse delivery using microdialysis) of the aromatase inhibitor fadrozole (FAD) into NCM transiently suppresses local estradiol levels (13). ResultsIn Vivo Retrodialysis and Behavior. Adult zebra finches express a robust behavioral preference for acoustic playback of their tutor's song or bird's own song (BOS) compared with conspecific male song (CON) (4, 5, 8), and be...

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Section: Discussionmentioning

confidence: 50%

Brain estrogens rapidly strengthen auditory encoding and guide song preference in a songbird

Remage‐Healey

Coleman

Oyama

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

191

224

View full text Add to dashboard Cite

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“…Some of these effects may represent adaptive mechanisms, allowing parents to adjust the developmental trajectories of their offspring to the environmental conditions in which they will subsequently live (Deng & Rogers 2002a;Andrew 2009). For example, maternal glucocorticoids deposited in the egg or crossing the placenta profoundly affect the development of lateralization (Diaz et al 1995;Rogers & Deng 2005), an effect that may enable the mother experiencing stress situations (such as predator attack) at the time of embryo formation to adaptively influence the laterality pattern of their offspring (Deng & Rogers 2002a;Halpern et al 2005).…”

Section: Discussionmentioning

confidence: 99%

The costs of hemispheric specialization in a fish

et al. 2009

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Laboratory and field studies have documented better cognitive performance associated with marked hemispheric specialization in organisms as diverse as chimpanzees, domestic chicks and topminnows. While providing an evolutionary explanation for the emergence of cerebral lateralization, this evidence represents a paradox because a large proportion of non-lateralized (NL) individuals is commonly observed in animal populations. Hemispheric specialization often determines large left -right differences in perceiving and responding to stimuli. Using topminnows selected for a high or low degree of lateralization, we tested the hypothesis that individuals with greater functional asymmetry pay a higher performance cost in situations requiring matching information from the two eyes. When trained to use the middle door in a row of a nine, NL fish correctly chose the central door in most cases, while lateralized fish showed systematic leftward or rightward biases. When choosing between two shoals, each seen with a different eye, NL fish chose the high-quality shoal significantly more often than the lateralized fish, whose performance was affected by eye preference for analysing social stimuli. These findings suggest the existence of a trade-off between computational advantages of hemispheric specialization and the ecological cost of making suboptimal decisions whenever relevant information is located on both sides of the body.

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“…At 12.00 h the next day, a Velcro-ringed cardboard cap was attached to the eye-ring around the left eye; bandage tape around the margin further reduced the input of ambient light to the eye. This method of monocular occlusion is frequently used in studies of brain lateralization [40]. Given that the avian brain is functionally lateralized [40], it is conceivable that the two hemispheres would respond differently to sleep loss [13,16,41].…”

Section: Methodsmentioning

confidence: 99%

Local sleep homeostasis in the avian brain: convergence of sleep function in mammals and birds?

et al. 2011

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The function of the brain activity that defines slow wave sleep (SWS) and rapid eye movement (REM) sleep in mammals is unknown. During SWS, the level of electroencephalogram slow wave activity (SWA or 0.5 -4.5 Hz power density) increases and decreases as a function of prior time spent awake and asleep, respectively. Such dynamics occur in response to waking brain use, as SWA increases locally in brain regions used more extensively during prior wakefulness. Thus, SWA is thought to reflect homeostatically regulated processes potentially tied to maintaining optimal brain functioning. Interestingly, birds also engage in SWS and REM sleep, a similarity that arose via convergent evolution, as sleeping reptiles and amphibians do not show similar brain activity. Although birds deprived of sleep show global increases in SWA during subsequent sleep, it is unclear whether avian sleep is likewise regulated locally. Here, we provide, to our knowledge, the first electrophysiological evidence for local sleep homeostasis in the avian brain. After staying awake watching David Attenborough's The Life of Birds with only one eye, SWA and the slope of slow waves (a purported marker of synaptic strength) increased only in the hyperpallium-a primary visual processing region-neurologically connected to the stimulated eye. Asymmetries were specific to the hyperpallium, as the non-visual mesopallium showed a symmetric increase in SWA and wave slope. Thus, hypotheses for the function of mammalian SWS that rely on local sleep homeostasis may apply also to birds.

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Lateralization of the Vertebrate Brain: Taking the Side of Model Systems: Figure 1.

Cited by 141 publications

References 84 publications

Brain estrogens rapidly strengthen auditory encoding and guide song preference in a songbird

Brain estrogens rapidly strengthen auditory encoding and guide song preference in a songbird

The costs of hemispheric specialization in a fish

Local sleep homeostasis in the avian brain: convergence of sleep function in mammals and birds?

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