Plasticity, the term we use to describe the ability of a nervous system to change with experience, is the evolutionary adaptation that freed animal behavior from the confines of genetic determinism. This capacity, which increases with brain complexity, is nowhere more evident than in vertebrates, especially mammals. Though the scientific study of brain plasticity dates back at least to the mid-19th century, the last several decades have seen unprecedented advances in the field afforded by new technologies. Olfaction is one system that has garnered particular attention in this realm because it is the only sensory modality with a lifelong supply of new neurons, from two niches no less! Here, we review some of the classical and contemporary literature dealing with the role of the stimulus or lack thereof in olfactory plasticity. We have restricted our comments to studies in mammals that have used dual tools of the field: stimulus deprivation and stimulus enrichment. The former manipulation has been implemented most frequently by unilateral naris occlusion and, thus, we have limited our comments to research using this technique. The work reviewed on deprivation provides substantial evidence of activity-dependent processes in both developing and adult mammals at multiple levels of the system from olfactory sensory neurons through to olfactory cortical areas. However, more recent evidence on the effects of deprivation also establishes several compensatory processes with mechanisms at every level of the system, whose function seems to be the restoration of information flow in the face of an impoverished signal. The results of sensory enrichment are more tentative, not least because of the actual manipulation: What odor or odors? At what concentrations? On what schedule? All of these have frequently not been sufficiently rationalized or characterized. Perhaps it is not surprising, then, that discrepant results are common in sensory enrichment studies. Despite this problem, evidence has accumulated that even passively encountered odors can “teach” olfactory cortical areas to better detect, discriminate, and more efficiently encode them for future encounters. We discuss these and other less-established roles for the stimulus in olfactory plasticity, culminating in our recommended “aspirations” for the field going forward.
This content will become publicly available on July 9, 2024
Activity-dependent neuronal plasticity is crucial for animals to adapt to dynamic sensory environments. Traditionally, it has been investigated using deprivation approaches in animal models primarily in sensory cortices. Nevertheless, emerging evidence emphasizes its significance in sensory organs and in sub-cortical regions where cranial nerves relay information to the brain. Additionally, critical questions started to arise. Do different sensory modalities share common cellular mechanisms for deprivation-induced plasticity at these central entry-points? Does the deprivation duration correlate with specific plasticity mechanisms?
This study systematically reviews and meta-analyses research papers that investigated visual, auditory, or olfactory deprivation in rodents of both sexes. It examines the consequences of sensory deprivation in homologous regions at the first central synapse following cranial nerve transmission (vision-lateral geniculate nucleus and superior colliculus; audition-ventral and dorsal cochlear nucleus; olfaction-olfactory bulb). The systematic search yielded 91 papers (39 vision, 22 audition, 30 olfaction), revealing substantial heterogeneity in publication trends, experimental methods, measures of plasticity, and reporting across the sensory modalities. Despite these differences, commonalities emerged when correlating plasticity mechanisms with the duration of sensory deprivation. Short-term deprivation (up to 1 day) reduced activity and increased disinhibition, medium-term deprivation (1 day to a week) involved glial changes and synaptic remodelling, and long-term deprivation (over a week) primarily led to structural alterations.
These findings underscore the importance of standardizing methodologies and reporting practices. Additionally, they highlight the value of cross-modals synthesis for understanding how the nervous system, including peripheral, pre-cortical, and cortical areas, respond to and compensate for sensory inputs loss.
- NSF-PAR ID:
- 10485328
- Publisher / Repository:
- DOI PREFIX: 10.1523
- Date Published:
- Journal Name:
- eneuro
- ISSN:
- 2373-2822
- Format(s):
- Medium: X Size: Article No. ENEURO.0435-23.2023
- Size(s):
- ["Article No. ENEURO.0435-23.2023"]
- Sponsoring Org:
- National Science Foundation
More Like this
-
Cheetham, Claire E. (Ed.)more » « less
-
Abstract Sensory input across modalities is highly dynamic, continuously confronting the brain with the task of making sense of the external world. Olfaction is a key sense that many species depend on for survival, for example to locate food sources and mating partners or to avoid encountering predators. In the absence of visual cues, olfactory cues are especially useful, as they provide information over a large range of distances. Natural odours form temporally complex plumes that show rapid fluctuations in odour concentration carrying information about the location of an odour source. This review focuses on how primarily mammals use this spatial information from olfactory cues to navigate their environment. I highlight progress made on the physical description of dynamically fluctuating odours, behavioural paradigms to investigate odour-guided navigation and review initial findings on the underlying neural mechanisms that allow mammals to extract spatial information from the dynamic odour landscape.more » « less
-
Synopsis Goal-directed learning is a key contributor to evolutionary fitness in animals. The neural mechanisms that mediate learning often involve the neuromodulator dopamine. In higher order cortical regions, most of what is known about dopamine’s role is derived from brain regions involved in motivation and decision-making, while significantly less is known about dopamine’s potential role in motor and/or sensory brain regions to guide performance. Research on rodents and primates represents over 95% of publications in the field, while little beyond basic anatomy is known in other vertebrate groups. This significantly limits our general understanding of how dopamine signaling systems have evolved as organisms adapt to their environments. This review takes a pan-vertebrate view of the literature on the role of dopamine in motor/sensory cortical regions, highlighting, when available, research on non-mammalian vertebrates. We provide a broad perspective on dopamine function and emphasize that dopamine-induced plasticity mechanisms are widespread across all cortical systems and associated with motor and sensory adaptations. The available evidence illustrates that there is a strong anatomical basis—dopamine fibers and receptor distributions—to hypothesize that pallial dopamine effects are widespread among vertebrates. Continued research progress in non-mammalian species will be crucial to further our understanding of how the dopamine system evolved to shape the diverse array of brain structures and behaviors among the vertebrate lineage.more » « less
-
more » « less
It has been postulated that the brain is organized by “metamodal,” sensory-independent cortical modules capable of performing tasks (e.g., word recognition) in both “standard” and novel sensory modalities. Still, this theory has primarily been tested in sensory-deprived individuals, with mixed evidence in neurotypical subjects, thereby limiting its support as a general principle of brain organization. Critically, current theories of metamodal processing do not specify requirements for successful metamodal processing at the level of neural representations. Specification at this level may be particularly important in neurotypical individuals, where novel sensory modalities must interface with existing representations for the standard sense. Here we hypothesized that effective metamodal engagement of a cortical area requires congruence between stimulus representations in the standard and novel sensory modalities in that region. To test this, we first used fMRI to identify bilateral auditory speech representations. We then trained 20 human participants (12 female) to recognize vibrotactile versions of auditory words using one of two auditory-to-vibrotactile algorithms. The vocoded algorithm attempted to match the encoding scheme of auditory speech while the token-based algorithm did not. Crucially, using fMRI, we found that only in the vocoded group did trained-vibrotactile stimuli recruit speech representations in the superior temporal gyrus and lead to increased coupling between them and somatosensory areas. Our results advance our understanding of brain organization by providing new insight into unlocking the metamodal potential of the brain, thereby benefitting the design of novel sensory substitution devices that aim to tap into existing processing streams in the brain.
SIGNIFICANCE STATEMENT It has been proposed that the brain is organized by “metamodal,” sensory-independent modules specialized for performing certain tasks. This idea has inspired therapeutic applications, such as sensory substitution devices, for example, enabling blind individuals “to see” by transforming visual input into soundscapes. Yet, other studies have failed to demonstrate metamodal engagement. Here, we tested the hypothesis that metamodal engagement in neurotypical individuals requires matching the encoding schemes between stimuli from the novel and standard sensory modalities. We trained two groups of subjects to recognize words generated by one of two auditory-to-vibrotactile transformations. Critically, only vibrotactile stimuli that were matched to the neural encoding of auditory speech engaged auditory speech areas after training. This suggests that matching encoding schemes is critical to unlocking the brain's metamodal potential. -
Avian cranial anatomy is constrained by the competing (or complementary) requirements and costs of various facial, muscular, sensory, and central neural structures. However, these constraints may operate differently in flighted versus flightless birds. We investigated cranial sense organ morphology in four lineages of flightless birds: kiwi (Apteryx), the Kakapo (Strigops habroptilus), and the extinct moa (Dinornithiformes) from New Zealand; and the extinct elephant birds from Madagascar (Aepyornithidae). Scleral ring and eye measurements suggest that the Upland Moa (Megalapteryx didinus) was diurnal, while measurements for the Kakapo are consistent with nocturnality. Kiwi are olfactory specialists, though here we postulate that retronasal olfaction is the dominant olfactory route in this lineage. We suggest that the Upland Moa and aepyornithids were also olfactory specialists; the former additionally displaying prominent bill tip sensory organs implicated in mechanoreception. Finally, the relative size of the endosseous cochlear duct revealed that the Upland Moa had a well-developed hearing sensitivity range, while the sensitivity of the kiwi, Kakapo, and aepyornithids was diminished. Together, our results reveal contrasting sensory strategies among extant and extinct flightless birds. More detailed characterisation of sensory capacities and cranial anatomy in extant birds may refine our ability to make accurate inferences about the sensory capacities of fossil taxa.more » « less
