Neuronal Adaptation to Visual Motion in Area MT of the Macaque

“Using compound stimuli composed of a preferred and null grating, Kohn and Movshon (2003) showed that null adaptation reduces the strength of opponent inhibition.”

“…MT responsiveness to the adapted direction is maintained whereas it is strongly reduced for nearby directions, leading to a sharpening of the tuning curve (Kohn and Movshon 2003; see Grill-Spector et al. 2006, for detailed discussion of various neural changes associated with stimulus repetition).”

“The retina is not the only part of the visual pathway involved in contrast processing, however, with contrast adaptation also taking place centrally in the striate cortex (V1) as well as extra-striate regions V2, V3 and human V4 (Ohzawa et al., 1985; Kohn and Movshon, 2003; Gardner et al., 2005).”

“The effects observed by Kohn and Movshon (2003, 2004) can also be attributed to adaptation early in the visual system, with the novel changes in MT tuning arising from an interaction between adapted feedforward input and unaltered recurrent excitatory and inhibitory connections within MT.”

“The horizontal shifts of contrast gain are similar to the changes in the sensitivity of individual neurons in monkey visual cortex seen after contrast adaptation (Allison et al. 1993; Carandini et al. 1997; Kohn and Movshon 2003; Sclar et al. 1989).”

“The subtractive term describes the suppressive surround with a Naka–Rushton model, where b and SIc50 are its response gain and contrast sensitivity, respectively (Kohn and Movshon, 2003).”

“One series of experiments (Lisberger and Movshon, 1999; Priebe and Lisberger, 2002; Priebe et al., 2002) studied short-term adaptation (recovery time constant of 86 ms; Priebe and Lisberger, 2002) that produces transient responses to motion stimuli in extrastriate area MT/V5 and concluded that this adaptation mechanis…”

“For instance, the complex receptive fields in the middle temporal cortical area in monkeys are thought to be a key neural substrate for the processing of visual motion (Britten et al., 1993; O’Keefe and Movshon, 1998; Grunewald et al., 2002; Kohn and Movshon, 2003; Osborne et al., 2004).”

“Sensory neurons that encode some particular attribute of a stimulus show progressively smaller responses when that attribute is repeated (Miller and Desimone, 1994; Kohn and Movshon, 2003).”

“…previously used to measure adaptation in electrophysiology and psychophysics experiments (Bradley et al. 1988; Carandini et al. 1997, 1998; De Valois 1977; Hammett and Snowden 1995; Kohn and Movshon 2003; Pantle and Sekuler 1968; Sclar et al. 1989; Snowden and Hammett 1996; Solomon et al. 2004).”

“…1982, 1985; Sclar et al., 1985), monkey and prosimian V1 (Allison et al., 1993; Carandini et al., 1997; Sclar et al., 1989), and monkey middle temporal area (MT; Kohn and Movshon, 2003) have revealed that adaptation to contrast results in mostly horizontal shifts of contrast response functions.”

“Sensory neurons that encode some particular attribute of a stimulus usually show progressively smaller responses when that attribute is repeated (Miller and Desimone, 1994; Kohn and Movshon, 2003).”

“A recent study of motion adaptation in MT neurons in anesthetized monkeys demonstrates an attractive shift in the direction tuning of these neurons, toward the adapting direction (Kohn and Movshon 2003, 2004).”

“Of the 5 studies that have examined motion adaptation in MT neurons (Kohn and Movshon 2003; Lisberger and Movshon 1999; Petersen et al. 1985; Priebe et al. 2002; Van Wezel and Britten 2002), none has specifically examined the activity during the interval that immediately followed the adapting…”

“Because of the spatial specificity of motion adaptation (Kohn and Movshon 2003), this reference pattern was therefore nonadapted.”

“For fMRI data analyses, because there was no qualitative difference between the ROI locations defined in different sessions, the fMRI data presented below are from the ROIs defined in the first event-related fMRI session.”

“…neural adaptation observed at various areas/levels in the visual systemVa likely possibility given the neuroimaging work by Culham et al. (1999), Kohn and Movshon (2003), Downloaded From: https://jov.arvojournals.org/pdfaccess.ashx?url=/data/journals/jov/932841/ on 11/17/2018 and Tootell et al.…”

“Alternatively, however, the classic timecourse of the identity aftereffect could be inherited from lower-level adaptation (cf. Kohn & Movshon, 2003).”

“…modified, adapted state of neurons that is thought to be the substrate of perceptual aftereffects (Clifford et al., 2007; Jin et al., 2005; Kohn & Movshon, 2003, 2004; Schwartz, Hsu, & Dayan, 2007) be transmitted horizontally through the brain in any direction and amplitude depending on the…”

“Cortical cells in area MT also express adaptation that is primarily caused by a presynaptic mechanism (Kohn and Movshon, 2003, 2004).”

“Nature adjusts the dynamics of cortical networks with a number of self-regulating local mechanisms involving complex networks of inhibitory neurons (E/ I balance) (134), normalization of synaptic strength (135), synaptic plasticity (136), adaptation (137), and membrane resonance (138).”

“Unlike the spatial specificity of prolonged grating adaptation within the RFs of individual MT neurons (suggesting inheritance from V1; Kohn and Movshon 2003), the effects of brief adaptation with dot fields transfers between subregions, suggesting a direct effect on MT cells (Priebe et al. 2002).”

“Single-unit recordings suggest, for example, that under some con- a fditions, adaptation observed in MT is mainly due to decreased input from V1 (Kohn and Movshon, 2003).”

“Motion aftereffects (MAE) are mediated to some extent by MT (Kohn & Movshon, 2003, 2004), an area specialized in motion analysis (Born & Bradley, 2005) and one group has claimed that a portion of the human extrastriate visual cortex encodes motion in spatiotopic (d’Avossa doi: 10 .1167 /9 .5 .16…”

“This result is consistent with previous reports that motion adaptation affects the contrast gain but not the response gain of MT neurons, resulting in strong modulation of responses to low-contrast test stimuli and weak effects at high contrast (14).”

“The presence of a motion aftereffect is therefore an indicator of the involvement of direction-selective neural mechanisms (Kohn & Movshon, 2003; Petersen, Baker, & Allman, 1985; Van Wezel & Britten, 2002).”

“For example, do face aftereffects depend on adaptation in neurons that directly encode the stimulus as a face? Identifying the sites of adaptation is difficult because sensitivity changes that arise early in the visual system will propagate to later stages, and, thus, complex aftereffects could reflect changes inherit…”

“It is worth noting that our results in young groups re somewhat different from Kohn and Movshon’s (2003) esults.”

“A decrease in contrast gain due to adaptation is also supported by results from neurophysiological studies that have directly compared pre- and post-adaptation CRFs in cat area 17 (Ohzawa, Sclar, & Freeman, 1985) and in motion area MT of macaque monkeys (Kohn & Movshon, 2003).”

“However, the results of another study using long adaptation (several seconds) led the authors to conclude that adaptation does not take place in the V5 at the earlier stages of motion processing [9].”

“One possibility is that stimuli preceding the flash in the outward bound trajectory might lead to short-term adaptation (Maffei et al., 1973; Bonds, 1991; Muller et al., 1999; Priebe et al., 2002; Kohn and Movshon, 2003).”

“Our results are in general agreement with previous studies of cascading adaptation measured physiologically (Kohn and Movshon, 2003, 2004).”

“The responses of neurons in area MT show adaptation, typically evident as reduced responsiveness after periods of elevated firing (Kohn and Movshon 2003, 2004; van Wezel and Britten 2002).”

“For instance, neurons in visual cortex change their responsivity and stimulus preferences following exposure to previous visual stimuli, commonly referred to as neural adaptation (Müller et al., 1999; Dragoi et al., 2000, 2001; Kohn and Movshon, 2003, 2004).”

“The Fisher information may be used for standardizing metrics of parameters (Amari & Nagaoka, 2000) on the basis of the Cramér-Rao bound, E[(θ − θ̄ )2] ≥ 1 nI (θ ) , (C.1) where n is the number of data.”

“…response elicited by a person with migraine may be comparable with another without migraine viewing a higher contrast pattern, analogous to the increase in firing rate with contrast that is observed in direction-selective cells in physiological studies (Maffei et al., 1973; Kohn and Movshon, 2003).”

“It is well known that the responses of many MT neurons diminish after prolonged stimulation (Petersen et al., 1985; Priebe and Lisberger, 2002; Priebe et al., 2002; Van Wezel and Britten, 2002; Kohn and Movshon, 2003; Krekelberg et al., 2006a).”

“Kohn and Movshon (2003) measured the contrast response functions of single neurones in macaque extrastriate area V5 (or MT) to their preferred sine wave grating stimuli, optimised for drift direction, spatial and temporal frequency, position and size.”

“Several studies have attempted to discern whether changes in sensitivity measured in one network could be explained by effects inherited from earlier areas or structures (Kohn and Movshon 2003; Movshon and Lennie 1979; Nelson 1991a, 1991b; Ohzawa et al. 1985; Priebe et al. 2002).”

“Intuitively, this might seem surprising, because adaptation is usually considered a low-level physiological process (e.g., Kohn, 2007), whereas serial dependence very often shows the hallmarks of a much higher-level effect (e.g., Fornaciai & Park, 2019b; Pascucci et al., 2019).”

“…many levels across the sensory processing pathways and at many timescales, and thus influences many aspects of perception (e.g., Brown & Masland, 2001; Boynton & Finney, 2003; Montaser-Kouhsari, Landy, Heeger, & Larsson, 2007; Kohn & Movshon, 2003; Kohn, 2007; Glasser, Tsui, Pack, & Tadin, 2011).”

“Whereas prolonged stimulation of an excitatory mechanism is believed to produce a subsequent reduction in its response (suppression), adapting an inhibitory mechanism has been found to reduce its inhibitory effect (disinhibition) (Durand, Freeman, & Carandini, 2007; Kohn & Movshon, 2003).”

“…exposure to a moving stimulus leads to a change in the responsiveness of motionsensitive neurons in the visual system (Barlow & Hill, 1963; Hammond, Mouat, & Smith, 1985; Kohn & Movshon, 2003; Petersen, Baker, & Allman, 1985; Van Wezel & Britten, 2002; von der Heydt, Hanny, & Adorjani, 1978).”

“In addition, facilitation of responses was a rare occurrence and no tuning shifts were recorded [42].”

“Others have shown direction selective reductions in gain (Kohn and Movshon, 2003; Patterson et al., 2014), and it is well established that we expect gain reductions proportional to the unit’s response to the adaptor in general (Solomon and Kohn, 2014).”

“When explaining the present effects, one needs to additionally consider that priming modifies the amount of external stimulation required to activate neuronal populations (e.g. Kohn and Movshon, 2003; Kohn, 2007).”

“…explanation suggests that RS is related to the local alteration of the synaptic inputs/spike frequency of the neurons (De Baene and Vogels, 2010; Kohn and Movshon, 2003; Priebe et al., 2002; Sawamura et al., 2006), the theory of predictive coding (PC) suggests the involvement of top-down…”

“This follows from the observation that neuronal responses are enhanced when a preferred motion stimulus is preceded by adapting motion in the opposite direction (van Wezel and Britten, 2002; Kohn and Movshon, 2003).”

“…mechanism of the MAE is probably a combination of (i) a change in the tuning curves of direction-selective neurons that encode the preferred direction of motion and (ii) a disinhibition of neurons that encode the opposite direction of motion (Krekelberg et al., 2006; Kohn & Movshon, 2003).”

“We did so because adaptation is known to have strong effects in V1, and because grating adaptation effects in MT are inherited from the early visual system (Kohn and Movshon 2003).”

“Adaptation refers to a change in the sensitivity of neurons after prolonged exposure to a particular stimulus (Kohn and Movshon 2003, 2004; Webster et al. 2007).”