Moving Sensory Adaptation beyond Suppressive Effects in Single Neurons

Solomon, Samuel G.; Kohn, Adam

doi:10.1016/j.cub.2014.09.001

Cited by 216 publications

(258 citation statements)

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“…Adaptation, which occurs throughout sensory systems, represents a form of experience-dependent plasticity in which our current sensory experience is intimately affected by how we viewed the world only moments before. It is widely held to pose numerous functional advantages (12)(13)(14)(15)(16), including serving to autocalibrate perceptual systems to their environment by dynamically tuning its responses to match the distribution of stimuli to make maximal use of the limited working range of the system (12)(13)(14)(15)(16). It achieves this by reducing the transmission of redundant information and maximizing sensitivity to relevant information.…”

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confidence: 99%

Children with autism spectrum disorder show reduced adaptation to number

Turi

Burr

Igliozzi

et al. 2015

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

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Autism is known to be associated with major perceptual atypicalities. We have recently proposed a general model to account for these atypicalities in Bayesian terms, suggesting that autistic individuals underuse predictive information or priors. We tested this idea by measuring adaptation to numerosity stimuli in children diagnosed with autism spectrum disorder (ASD). After exposure to large numbers of items, stimuli with fewer items appear to be less numerous (and vice versa). We found that children with ASD adapted much less to numerosity than typically developing children, although their precision for numerosity discrimination was similar to that of the typical group. This result reinforces recent findings showing reduced adaptation to facial identity in ASD and goes on to show that reduced adaptation is not unique to faces (social stimuli with special significance in autism), but occurs more generally, for both parietal and temporal functions, probably reflecting inefficiencies in the adaptive interpretation of sensory signals. These results provide strong support for the Bayesian theories of autism.utism is a heritable, lifelong neurodevelopmental condition with striking effects on social communication. The condition, however, is also associated with a range of nonsocial symptoms, including both hypersensitivity and hyposensitivity to perceptual stimuli, and sensory-seeking behaviors such as attraction to light, intense looking at objects, and fascination with brightly colored objects. These sensory atypicalities, which now form part of the diagnostic criteria for autism (1), can have debilitating effects on the lives of autistic people (2) and their families (3).We have recently proposed a Bayesian account of autism (4), suggesting that it is not sensory processing itself that is disrupted in individuals with autism, but the interpretation of the sensory input. The Bayesian class of theories, including predictive coding and other generative models (5-7), assumes that perception is an optimized combination of external sensory data (the likelihood) and an internal model (the prior). We suggested that this process may be atypical in autism, in that the internal priors are underweighted and less used than in typical individuals. Our theory has been followed by several others along similar lines (8-11).The suggestion of underutilization of priors leads to several specific predictions. One strong prediction is that autistic individuals should show reduced adaptation aftereffects. Adaptation, which occurs throughout sensory systems, represents a form of experience-dependent plasticity in which our current sensory experience is intimately affected by how we viewed the world only moments before. It is widely held to pose numerous functional advantages (12-16), including serving to autocalibrate perceptual systems to their environment by dynamically tuning its responses to match the distribution of stimuli to make maximal use of the limited working range of the system (12-16). It achieves this by reducing the transm...

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confidence: 99%

Children with autism spectrum disorder show reduced adaptation to number

Turi

Burr

Igliozzi

et al. 2015

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

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“…Alternatively, if the CEs in the LPFC reflect repetition suppression (Miller et al, 1993;Woloszyn and Sheinberg, 2009) Solomon and Kohn, 2014), these processes would weaken or disappear with spatially nonoverlapping S1 and S2. However, this is unlikely for several reasons.…”

Section: Contralateral Responses Dominate But Only Early In the Trialmentioning

confidence: 99%

Prefrontal Neurons Represent Motion Signals from Across the Visual Field But for Memory-Guided Comparisons Depend on Neurons Providing These Signals

2016

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Visual decisions often involve comparisons of sequential stimuli that can appear at any location in the visual field. The lateral prefrontal cortex (LPFC) in nonhuman primates, shown to play an important role in such comparisons, receives information about contralateral stimuli directly from sensory neurons in the same hemisphere, and about ipsilateral stimuli indirectly from neurons in the opposite hemisphere. This asymmetry of sensory inputs into the LPFC poses the question of whether and how its neurons incorporate sensory information arriving from the two hemispheres during memory-guided comparisons of visual motion. We found that, although responses of individual LPFC neurons to contralateral stimuli were stronger and emerged 40 ms earlier, they carried remarkably similar signals about motion direction in the two hemifields, with comparable direction selectivity and similar direction preferences. This similarity was also apparent around the time of the comparison between the current and remembered stimulus because both ipsilateral and contralateral responses showed similar signals reflecting the remembered direction. However, despite availability in the LPFC of motion information from across the visual field, these "comparison effects" required for the comparison stimuli to appear at the same retinal location. This strict dependence on spatial overlap of the comparison stimuli suggests participation of neurons with localized receptive fields in the comparison process. These results suggest that while LPFC incorporates many key aspects of the information arriving from sensory neurons residing in opposite hemispheres, it continues relying on the interactions with these neurons at the time of generating signals leading to successful perceptual decisions.

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“…Barlow and Hill (1963) and Miller, Gochin, and Gross (1991)), repeated presentation of a stimulus tends to elicit a response smaller than the initial presentation. is good evidence for more complex effects on tuning curves and population interactions (Clifford et al, , 2000Kohn & Movshon, 2004;Solomon & Kohn, 2014).…”

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confidence: 89%

“…This is an example of a tilt aftereffect (Gibson, 1937;Gibson & Radner, 1937;Vernon, 1934). Aftereffects are thought to be caused by neural adaptation -changes in the responsiveness of neurons following prolonged stimulation (Barlow & Hill, 1963;Clifford et al, 2007;Krekelberg, Boynton, & van Wezel, 2006;Solomon & Kohn, 2014;Thompson & Burr, 2009;Wark, Lundstrom, & Fairhall, 2007).…”

Section: H a P T E R : Introductionmentioning

confidence: 99%

“…Because encoding schemes involving different arrangements of neurons can predict different patterns of perceptual changes after adaptation, aftereffects can provide insight into how relevant stimulus dimensions are encoded (Clifford, Wenderoth, & Spehar, 2000;Mollon, 1977;Solomon & Kohn, 2014;Webster, 2011). For instance, the study of aftereffects has contributed much to our current knowledge of how the brain encodes colour (see Webster (1996)), motion (see Anstis, Verstraten, and Mather (1998)), orientation (see Clifford, Wyatt, Arnold, Smith, and Wenderoth (2001)), and spatial frequency (see Blakemore and Campbell (1969) and Blakemore, Nachmias, and Sutton (1970)).…”

Section: H a P T E R : Introductionmentioning

confidence: 99%

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Norms are Not the Norm: Testing Theories of Sensory Encoding Using Visual Aftereffects

Storrs¹

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A thesis submitted for the degree of Doctor of Philosophy at the University of Queensland in 2015School of Psychology A B S T R A C TThe goal of visual neuroscience is to explain how patterns of neural activity give rise to visual experiences. Here I use visual aftereffects to explore the computational principles underlying the perception of simple, intermediate, and complex forms (orientations, shapes, and faces). Aftereffects occur when exposure to one stimulus changes the appearance of a subsequent stimulus. In the tilt aftereffect, for example, staring at a left-tilted line can make a vertical line seem briefly to lean to the right. Aftereffects are thought to be caused by neural adaptation -changes in the responsiveness of neurons after prolonged stimulation.Visual aftereffects allow us to probe sensory encoding, because adaptation within different encoding schemes can predict different patterns of perceptual aftereffect. I focus on two theories of encoding prominent in the face recognition literature. According to norm-based accounts, faces are represented in terms of how they deviate from a unique norm, such as the average of all experienced faces. Similar proposals have been raised in other contexts, for example to encode the aspect ratio of shapes. Norm-based encoding can be implemented by a population in which neurons respond increasingly as a stimulus moves further in the neuron's preferred direction, away from a normative value in stimulus space. Alternatively, exemplar-based accounts propose that faces are encoded in terms of their similarity to a number of previously-experienced exemplars. Exemplar-based encoding can be implemented by a population of non-monotonically tuned neurons that prefer particular points in stimulus space, rather than directions.Norm-based and exemplar-based accounts make distinct predictions for the pattern of aftereffects one should experience following adaptation. Norm-based encoding is associated with renormalisation, in which the adapting stimulus appears more 'neutral' or 'average' after prolonged viewing, and the appearances of other stimuli are altered in the same fashion (e.g. after adapting to a male face, all faces should look more feminine).Exemplar-based encoding is associated with 'local repulsion,' in which the adapting stimulus appears unchanged, but differences between it and subsequent stimuli are exaggerated (e.g. after adapting to a male face, a very masculine face should look even more masculine, while an androgynous or female face should look more feminine).Over the past fifteen years, norm-based theories of shape and face encoding have gained traction, ostensibly supported by evidence from aftereffects. In Chapter 1, I review this evidence, and relate it to an older debate concerning the role of norms in orientation perception. I conclude that the evidence for renormalisation in form perception is under-2 3 whelming. In Chapter 2 I empirically address the most recent evidence for orientation renormalisation. I show that these data likely arise from an ...

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Moving Sensory Adaptation beyond Suppressive Effects in Single Neurons

Cited by 216 publications

References 141 publications

Children with autism spectrum disorder show reduced adaptation to number

Children with autism spectrum disorder show reduced adaptation to number

Prefrontal Neurons Represent Motion Signals from Across the Visual Field But for Memory-Guided Comparisons Depend on Neurons Providing These Signals

Norms are Not the Norm: Testing Theories of Sensory Encoding Using Visual Aftereffects

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