High internal noise and poor external noise filtering characterize perception in autism spectrum disorder.
ABSTRACT: An emerging hypothesis postulates that internal noise is a key factor influencing perceptual abilities in autism spectrum disorder (ASD). Given fundamental and inescapable effects of noise on nearly all aspects of neural processing, this could be a critical abnormality with broad implications for perception, behavior, and cognition. However, this proposal has been challenged by both theoretical and empirical studies. A crucial question is whether and how internal noise limits perception in ASD, independently from other sources of perceptual inefficiency, such as the ability to filter out external noise. Here, we separately estimated internal noise and external noise filtering in ASD. In children and adolescents with and without ASD, we computationally modeled individuals' visual orientation discrimination in the presence of varying levels of external noise. The results revealed increased internal noise and worse external noise filtering in individuals with ASD. For both factors, we also observed high inter-individual variability in ASD, with only the internal noise estimates significantly correlating with severity of ASD symptoms. We provide evidence for reduced perceptual efficiency in ASD that is due to both increased internal noise and worse external noise filtering, while highlighting internal noise as a possible contributing factor to variability in ASD symptoms.
Project description:Human perception is invariably accompanied by a graded feeling of confidence that guides metacognitive awareness and decision-making. It is often assumed that this arises solely from the feed-forward encoding of the strength or precision of sensory inputs. In contrast, interoceptive inference models suggest that confidence reflects a weighted integration of sensory precision and expectations about internal states, such as arousal. Here we test this hypothesis using a novel psychophysical paradigm, in which unseen disgust-cues induced unexpected, unconscious arousal just before participants discriminated motion signals of variable precision. Across measures of perceptual bias, uncertainty, and physiological arousal we found that arousing disgust cues modulated the encoding of sensory noise. Furthermore, the degree to which trial-by-trial pupil fluctuations encoded this nonlinear interaction correlated with trial level confidence. Our results suggest that unexpected arousal regulates perceptual precision, such that subjective confidence reflects the integration of both external sensory and internal, embodied states.
Project description:Damage to the primary visual cortex typically causes cortical blindness (CB) in the hemifield contralateral to the damaged hemisphere. Recent evidence indicates that visual training can partially reverse CB at trained locations. Whereas training induces near-complete recovery of coarse direction and orientation discriminations, deficits in fine motion processing remain. Here, we systematically disentangle components of the perceptual inefficiencies present in CB fields before and after coarse direction discrimination training. In seven human CB subjects, we measured threshold versus noise functions before and after coarse direction discrimination training in the blind field and at corresponding intact field locations. Threshold versus noise functions were analyzed within the framework of the linear amplifier model and the perceptual template model. Linear amplifier model analysis identified internal noise as a key factor differentiating motion processing across the tested areas, with visual training reducing internal noise in the blind field. Differences in internal noise also explained residual perceptual deficits at retrained locations. These findings were confirmed with perceptual template model analysis, which further revealed that the major residual deficits between retrained and intact field locations could be explained by differences in internal additive noise. There were no significant differences in multiplicative noise or the ability to process external noise. Together, these results highlight the critical role of altered internal noise processing in mediating training-induced visual recovery in CB fields, and may explain residual perceptual deficits relative to intact regions of the visual field.
Project description:Neural systems are inherently noisy, and this noise can affect our perception from moment to moment. This is particularly apparent in binocular rivalry, where perception of competing stimuli shown to the left and right eyes alternates over time. We modulated rivalling stimuli using dynamic sequences of external noise of various rates and amplitudes. We repeated each external noise sequence twice, and assessed the consistency of percepts across repetitions. External noise modulations of sufficiently high contrast increased consistency scores above baseline, and were most effective at 1/8Hz. A computational model of rivalry in which internal noise has a 1/f (pink) temporal amplitude spectrum, and a standard deviation of 16% contrast, provided the best account of our data. Our novel technique provides detailed estimates of the dynamic properties of internal noise during binocular rivalry, and by extension the stochastic processes that drive our perception and other types of spontaneous brain activity.
Project description:Perceptual processing in autism spectrum disorder (ASD) is marked by superior low-level task performance and inferior complex-task performance. This observation has led to theories of defective integration in ASD of local parts into a global percept. Despite mixed experimental results, this notion maintains widespread influence and has also motivated recent theories of defective multisensory integration in ASD. Impaired ASD performance in tasks involving classic random dot visual motion stimuli, corrupted by noise as a means to manipulate task difficulty, is frequently interpreted to support this notion of global integration deficits. By manipulating task difficulty independently of visual stimulus noise, here we test the hypothesis that heightened sensitivity to noise, rather than integration deficits, may characterize ASD. We found that although perception of visual motion through a cloud of dots was unimpaired without noise, the addition of stimulus noise significantly affected adolescents with ASD, more than controls. Strikingly, individuals with ASD demonstrated intact multisensory (visual-vestibular) integration, even in the presence of noise. Additionally, when vestibular motion was paired with pure visual noise, individuals with ASD demonstrated a different strategy than controls, marked by reduced flexibility. This result could be simulated by using attenuated (less reliable) and inflexible (not experience-dependent) Bayesian priors in ASD. These findings question widespread theories of impaired global and multisensory integration in ASD. Rather, they implicate increased sensitivity to sensory noise and less use of prior knowledge in ASD, suggesting increased reliance on incoming sensory information.
Project description:Perceptual decision making is prone to errors, especially near threshold. Physiological, behavioural and modeling studies suggest this is due to the intrinsic or 'internal' noise in neural systems, which derives from a mixture of bottom-up and top-down sources. We show here that internal noise can form the basis of perceptual decision making when the external signal lacks the required information for the decision. We recorded electroencephalographic (EEG) activity in listeners attempting to discriminate between identical tones. Since the acoustic signal was constant, bottom-up and top-down influences were under experimental control. We found that early cortical responses to the identical stimuli varied in global field power and topography according to the perceptual decision made, and activity preceding stimulus presentation could predict both later activity and behavioural decision. Our results suggest that activity variations induced by internal noise of both sensory and cognitive origin are sufficient to drive discrimination judgments.
Project description:Biological systems are often subject to external noise from signal stimuli and environmental perturbations, as well as noises in the intracellular signal transduction pathway. Can different stochastic fluctuations interact to give rise to new emerging behaviors? How can a system reduce noise effects while still being capable of detecting changes in the input signal? Here, we study analytically and computationally the role of nonlinear feedback systems in controlling external noise with the presence of large internal noise. In addition to noise attenuation, we analyze derivatives of Fano factor to study systems' capability of differentiating signal inputs. We find effects of internal noise and external noise may be separated in one slow positive feedback loop system; in particular, the slow loop can decrease external noise and increase robustness of signaling with respect to fluctuations in rate constants, while maintaining the signal output specific to the input. For two feedback loops, we demonstrate that the influence of external noise mainly depends on how the fast loop responds to fluctuations in the input and the slow loop plays a limited role in determining the signal precision. Furthermore, in a dual loop system of one positive feedback and one negative feedback, a slower positive feedback always leads to better noise attenuation; in contrast, a slower negative feedback may not be more beneficial. Our results reveal interesting stochastic effects for systems containing both extrinsic and intrinsic noises, suggesting novel noise filtering strategies in inherently stochastic systems.
Project description:We combined an external noise paradigm with an efficient procedure for obtaining contrast thresholds (Lesmes et al., 2006) in order to model developmental changes in the effect of noise on contrast discrimination during childhood. Specifically, we measured the contrast thresholds of 5-, 7-, 9-year-olds and adults (n = 20/age) in a two alternative forced-choice orientation discrimination task over a wide range of external noise levels and at three levels of accuracy. Overall, as age increased, contrast thresholds decreased over the entire range of external noise levels tested. The decrease was greatest between 5 and 7 years of age. The reduction in threshold after age 5 was greater in the high than the low external noise region, a pattern implying greater tolerance of the irrelevant background noise as children became older. To model the mechanisms underlying these developmental changes in terms of internal noise components, we adapted the original perceptual template model (Lu and Dosher, 1998) and normalized the magnitude of performance changes against the performance of 5-year-olds. The resulting model provided an excellent fit (r (2) = 0.985) to the contrast thresholds at multiple levels of accuracy (60, 75, and 90%) across a wide range of external noise levels. The improvements in contrast thresholds with age were best modeled by a combination of reductions in internal additive noise, reductions in internal multiplicative noise, and improvements in excluding external noise by template retuning. In line with the data, the improvement was greatest between 5 and 7 years of age, accompanied by a 39% reduction in additive noise, 71% reduction in multiplicative noise, and 45% improvement in external noise exclusion. The modeled improvements likely reflect developmental changes at the cortical level, rather than changes in front-end structural properties (Kiorpes et al., 2003).
Project description:Autism spectrum disorder (ASD) is associated with noise hypersensitivity, the suboptimal extraction of meaningful signals in noisy environments. Because sensory filtering can involve distinct automatic and executive circuit mechanisms, however, developing circuit-specific therapeutic strategies for ASD noise hypersensitivity can be challenging. Here, we find that both of these processes are individually perturbed in one monogenic form of ASD, Ptchd1 deletion. Although Ptchd1 is preferentially expressed in the thalamic reticular nucleus during development, pharmacological rescue of thalamic perturbations in knockout (KO) mice only normalized automatic sensory filtering. By discovering a separate prefrontal perturbation in these animals and adopting a combinatorial pharmacological approach that also rescued its associated goal-directed noise filtering deficit, we achieved full normalization of noise hypersensitivity in this model. Overall, our work highlights the importance of identifying large-scale functional circuit architectures and utilizing them as access points for behavioral disease correction.
Project description:Much of our daily communication occurs in the presence of background noise, compromising our ability to hear. While understanding speech in noise is a challenge for everyone, it becomes increasingly difficult as we age. Although aging is generally accompanied by hearing loss, this perceptual decline cannot fully account for the difficulties experienced by older adults for hearing in noise. Decreased cognitive skills concurrent with reduced perceptual acuity are thought to contribute to the difficulty older adults experience understanding speech in noise. Given that musical experience positively impacts speech perception in noise in young adults (ages 18-30), we asked whether musical experience benefits an older cohort of musicians (ages 45-65), potentially offsetting the age-related decline in speech-in-noise perceptual abilities and associated cognitive function (i.e., working memory). Consistent with performance in young adults, older musicians demonstrated enhanced speech-in-noise perception relative to nonmusicians along with greater auditory, but not visual, working memory capacity. By demonstrating that speech-in-noise perception and related cognitive function are enhanced in older musicians, our results imply that musical training may reduce the impact of age-related auditory decline.
Project description:Cells sense chemical spatial gradients and respond by polarizing internal components. This process can be disrupted by gradient noise caused by fluctuations in chemical concentration.We investigated how external gradient noise affects spatial sensing and response focusing on noise-filtering and the resultant tradeoffs. First, using a coarse-grained mathematical model of gradient-sensing and cell polarity, we characterized three negative consequences of noise: Inhibition of the extent of polarization, degradation of directional accuracy, and production of a noisy output polarization. Next, we explored filtering strategies and discovered that a combination of positive feedback, multiple signaling stages, and time-averaging produced good results. There was an important tradeoff, however, because filtering resulted in slower polarization. Simulations demonstrated that a two-stage filter-amplifier resulted in a balanced outcome. Then, we analyzed the effect of noise on a mechanistic model of yeast cell polarization in response to gradients of mating pheromone. This analysis showed that yeast cells likely also combine the above three filtering mechanisms into a filter-amplifier structure to achieve impressive spatial-noise tolerance, but with the consequence of a slow response time. Further investigation of the amplifier architecture revealed two positive feedback loops, a fast inner and a slow outer, both of which contributed to noise-tolerant polarization. This model also made specific predictions about how orientation performance depended upon the ratio between the gradient slope (signal) and the noise variance. To test these predictions, we performed microfluidics experiments measuring the ability of yeast cells to orient to shallow gradients of mating pheromone. The results of these experiments agreed well with the modeling predictions, demonstrating that yeast cells can sense gradients shallower than 0.1% ?m-1, approximately a single receptor-ligand molecule difference between front and back, on par with motile eukaryotic cells.Spatial noise impedes the extent, accuracy, and smoothness of cell polarization. A combined filtering strategy implemented by a filter-amplifier architecture with slow dynamics was effective. Modeling and experimental data suggest that yeast cells employ these elaborate mechanisms to filter gradient noise resulting in a slow but relatively accurate polarization response.