Neuronal Adaptation to Visual Motion in Area MT of the Macaque

“(3) Our results also support those single-cell recording studies that suggest that short- and long-term adaptation have entirely different neural mechanisms (Priebe et al., 2002; Kohn and Movshon, 2003; Patterson et al., 2013).”

“However, adaptation occurs at several levels of visual processing (Hills, 2013; Kohn & Movshon, 2003), and other researchers have argued that number adaptation is instead a by-product of density adaptation (Dakin et al., 2011; Durgin, 2008).”

“This could be interpreted as evidence that a weaker motion signal is seen less often in the back, since motion adaptation reduces neural activity in area MT (Kohn & Movshon, 2003, 2004; Van Wezel & Britten, 2002).”

“Because the MAE is thought to be mediated by adaptation in low-level motion areas, specifically in neurons of the middle temporal (MT) area or earlier (see Kohn & Movshon , 2003; Tootell et al., 1995; Van Wezel & Britten, motion by low-level mechanisms.”

“…in postadaptation detection thresholds, reflects stronger neural activity in response to the adapting stimulus (Blake et al. 2006; Blakemore and Campbell 1969; Carandini et al. 1998; Dragoi et al. 2000; Engel 2005; Fang et al. 2005; Kohn and Movshon 2003; Larsson et al. 2006; Priebe et al. 2002).”

“These findings show that the adaptation following training is not only location- and orientation-specific, in accordance with classic adaptation reports (Blakemore & Nachmias, 1971; Kohn & Movshon, 2003)—but is also task dependent.”

“As previous studies have shown (Kohn & Movshon, 2003, 2004; Li et al., 2017; Patterson et al., 2014), adaptation could impact both V1 and V2 in parallel, but V2, receiving a major input from V1, following a feedforward hierarchical processing stream, may exhibit an enhanced effect.”

“…rare, which makes sense because continuous signaling of a stationary stimulus carries redundancy, and indeed most often responses to continuous stimuli adapt away (de Ruyter van Steveninck et al., 1986; Borst and Egelhaaf, 1987; Kohn and Movshon, 2003; Solomon et al., 2004; Safran et al., 2007).”

“This difference in magnitude is clearly consonant with a view in which the motion aftereffect is driven mainly by translation-based mechanisms in striate cortex (Kohn & Movshon 2003); mechanisms that fractal rotation fails to adapt.”

“This idea is strengthened by the fact that area MT also plays a role in the motion-aftereffect illusion (Kohn and Movshon, 2003), which is tightly related to motion adaptation and prediction.”

“This is well documented by the various neural response changes that occur after prolonged exposure to, for example, a fixed visual orientation [1–3] or motion direction stimulus [4,5], but also the corresponding perceptual changes [6–8].”

“This was confirmed more recently in area MT of macaque monkeys as well (Kohn and Movshon, 2003).”

“It is thought that the static MAE reXects neural adaptation of low-level motion-sensitive neurons (Ashida & Osaka, 1995; Kohn & Movshon, 2003; Nishida & Sato, 1995; von Grunau, 2002), with cortical areas V1 and V2 (which are rich in local motion detectors) identiWed as likely sites.”

“…and the physiological basis of the MAE as yet have relied on single-unit recordings from the visual cortex of monkeys (Petersen et al., 1985; Kohn and Movshon, 2003) and fMRI (Tootell et al., 1995; He et al., 1998; Culham et al., 1999; Taylor et al., 2000) and PET (Hautzel et al., 2001)…”

“A related difference between fly and macaque motion-sensitive cells has been reported for long-lasting adaptors: in this case MT neurons adapt only locally (Kohn and Movshon, 2003), whereas fly neurons display some degree of global adaptation (Neri and Laughlin, 2005).”

“MT is suggested to have a role in the anticipatory influence on the position map, however MT neurons’ responses saturate at low contrasts (Kohn & Movshon, 2003) and contrast dependent gain modulations due to motion require additional neural substrates.”

“This is comparable to the contrast response function of neurons in macaque area MT ( Heuer and Britten, 2002 ; Kohn and Movshon, 2003 ; Sclar et al., 1990 ).”

“A wellknown property of contrast–response is that it shifts horizontally with adaptation to center around the adapting contrast (Ohzawa et al., 1982, 1985; Sclar et al., 1985; Bonds, 1991; Kohn and Movshon, 2003; Solomon et al., 2004).”

“…effect) of the visual adaptation effect was proposed from a line of studies, which suggests Frontiers in Neuroscience | www.frontiersin.org 1 October 2019 | Volume 13 | Article 1039 that plasticity accumulates along the bottom–up stream (Kohn and Movshon, 2003; Dhruv and Carandini, 2014).”

“…single cell recordings in the middle temporal (MT) visual cortex of monkeys have shown that, following adaptation to a moving pattern, there is an induced imbalance in the activation of directional-selective neurons (Kohn and Movshon, 2003; Petersen et al., 1985; van Wezel and Britten, 2002).”

“There is substantial neurophysiological evidence for adaptation affecting the response of motion detectors in both V1 (Giaschi, Douglas, Marlin, & Cynader, 1993; Vautin & Berkley, 1977) and MT (Huk, Ress, & Heeger, 2001; Kohn & Movshon, 2003; Priebe, Churchland, & Lisberger, 2002; Tolias, Smirnakis, Augath, Trinath, &…”

“…features of adaptation observed in their large movement-detecting lobula plate tangential cells (LPTCs) are very similar to those observed in primate visual systems (Kohn & Movshon, 2003) and because the size and accessibility of these cells makes them amenable to electrophysiological recordings.”

“We used the following equation to analyze the data, which has been proved to well fit for the CRFs of cells of visual cortex in the cat and monkey (Albrecht and Hamilton, 1982; Kohn and Movshon, 2003): R 1⁄4 Rmax ð C n CnþCn50 Þ þM where R is the neuronal response to contrast C, Rmax is the neuronal maximum attainable…”

“Moreover, Kohn and Movshon (2003) showed that the MAE mechanism is realized within the motion pathway and not the form pathway.”

“Theoretical work also suggested that contrast adaptation in the mammalian visual system (Baccus and Meister, 2002; Carandini, 2000; Kohn and Movshon, 2003; Ohzawa et al., 1985; Solomon et al., 2004) could be understood as a consequence of the infomax principle (Adorján et al.”

“…& Intrilligator, 1996), binocular rivalry (Wade & Wenderoth, 1978) and continuous flash suppression (Maruya, Watanabe & Watanabe, 2008) and neural adaptation can be observed in anesthetized animals (Kohn & Movshon, 2003), suggesting that adaptation can occur in the absence of attentional selection.”

“The experiment is fully described in Kohn and Movshon (2003).”

“Neurons in the middle temporal area (MT) are tuned to the speed and direction of motion (Kohn and Movshon 2003; Born and Bradley 2005; Smith 2012).”

“Spatial adaptation appears to affect both contrast and response gain in primary visual cortex [16], whereas motion adaptation is mostly attributable to contrast gain in area MT [17].”

“We obtained thresholds at more than one level of test contrast (marked as black and gray symbols in Figures 2, 3, 5, and 6) because adaptation effects might vary in magnitude depending on the contrast of test stimuli due to changes in contrast gain (Kohn & Movshon, 2003).”

“To account for the data, there was no need to build in more subtle adaptation-induced changes to neuronal response properties, such as change in the width of the direction-tuning function (Yang & Lisberger, 2009) or shift in preferred direction (Kohn & Movshon, 2003).”

“…feature might be the mean luminance or contrast, or statistical properties of higher-order, such as spatial patterns or movements in particular directions (Baccus and Meister, 2002; Chung et al., 2002; Kohn and Movshon, 2003; Levy et al., 2013; Solomon and Kohn, 2014; Whitmire and Stanley, 2016).”

“Neurophysiological studies have found that neurons in the visual cortex change their response profiles after adaptation (Dragoi, Sharma, & Sur, 2000; Kohn & Movshon, 2003; Kohn & Movshon, 2004).”

“The improved performance for repeated stimuli can thus be the result of facilitated neural processing, which may manifest as an overall reduction in the amplitude of neuronal activation (Dragoi et al., 2002; Kohn and Movshon, 2003), a sharpening of response tuning in local networks of neurons (Wiggs and Martin, 1998;…”

“We used an adaptation paradigm similar to that used by Kohn and Movshon (2003) and Nishida et al. (1997) to investigate cross-stimulus adaptation effects on processing of optic flow and scale change.”

“31,32 For example, the simplest form of MAE is believed to arise when prior adaptation biases the response of V1 motion selective neurons to a static image, and this activity is then propagated forward (the majority of inputs to V5/MT are feedforward 30 ), causing the static image to appear as if…”

“The objective of the study, fully described in Kohn and Movshon (2003), is the exploration of how the neural activity changes with the direction of the stimulus.”

“…due to effects such as repetition suppression ( Dobbins et al., 2004; Grill-Spector et al., 2006) or contrast adaptation ( Gardner et al., 2005; Kohn & Movshon, 2003; Ohzawa et al., 1982, 1985), our analysis and modeling suggest that the typical strategy of averaging over repeats can overcome…”

“The motion aftereffect therefore provides indirect evidence for the existence of direction-selective neural mechanisms (Kohn & Movshon, 2003; Petersen, Baker, & Allman, 1985; Van Wezel & Britten, 2002).”

“For such simple stimuli, it has been shown that inherited input from V1 plays a significant role (Kohn and Movshon, 2003).”

“Similarly, spatial specificity has been found in visual motion adaptation in relation to neuronal activity in area MT (Kohn and Movshon 2003).”

“…been reported in the auditory cortex (Gourévitch and Eggermont 2008; Briley and Krumbholz 2013; Lanting et al. 2013), the middle temporal (MT) area (Kohn and Movshon 2003, 2004) and other brain regions (Merzenich et al. 1984; Armstrong-James et al. 1994; Webster and Mollon 1995; Karni and Bertini…”

“…in our task paradigm already suggests that the perceptual biases do not happen in the early stages of visual processing (such as the primary visual cortex), where the receptive fields of neurons are relatively small and the adaptation effect is strictly localized (Kohn, 2007; Kohn & Movshon, 2003).”

“Looking beyond human perception, such historical effects of background motion have also been established in primates; however, these studies exposed animals to non-natural moving stimuli, such as drifting sine wave gratings (Glasser et al. 2011; Kohn and Movshon 2003).”

“A second limitation derives from the observation that adaptation effects in downstream cortical regions can be inherited from upstream regions (Kohn and Movshon, 2003; Larsson and Harrison, 2015).”

“Visual and somatosensory neurons exhibit SSA in both spatial (Kohn and Movshon, 2003; Liu et al., 2017) or non-spatial (Movshon and Lennie, 1979; Maravall et al., 2007) domains.”