Evidence for MID processing in MT

In line with the idea that MID processing may be multiplexed in pathways known to underlie 2D motion and stereoscopic depth perception, two separate groups have recently published evidence for 3D motion tuning in MT neurons. Czuba et al., and Sanada and DeAngelis, conducted extracellular recordings in macaque MT. Using random dot stimuli containing CD and IOVD cues, both groups found that around 50% of all cells in MT selectively coded for motion directly towards or away from the observer (Czuba, Huk, Cormack, & Kohn, 2014; Sanada & DeAngelis, 2014), with a further subset of neurons showing a MID bias (Czuba et al., 2014). Thus in total, around 70% of neurons in MT could represent information about 3D motion. The majority of these were selective for IOVD cues, with relatively little contribution from CD (Sanada & DeAngelis, 2014). Additionally, MID

40

tuning was found to arise from different monocular motion preferences, as well as from nonlinear interactions of these signals when both eyes were stimulated (Czuba et al., 2014).

These results contradict earlier electrophysiological work (Maunsell & Van Essen, 1983) that found little evidence for neurons tuned to MID in this region. Maunsell and Van Essen found that their MID responses could be fully accounted for by separable contributions from 2D motion direction and static disparity. However, their recordings were focused on extending tuning for frontoparallel motion to the third dimension – in other words, they defined their MID vectors by the preferred lateral motion component of individual units. This means that the majority of their stimuli were not moving directly towards and away from the observer. Czuba et al. found that there was an overrepresentation of trajectories directly approaching or receding the observer, which may explain why Maunsell and Van Essen did not record a significant number of MID tuned units.

Direct evidence from extracellular recordings in macaque MT dovetails with indirect evidence using functional magnetic resonance imaging (fMRI) in humans. To date, three fMRI papers have shown that responses in cortical regions in or around human area hMT+ are modulated by MID stimuli containing CD and IOVD cues (Joo, Czuba, Cormack, & Huk, 2016; Rokers, Cormack, & Huk, 2009), or CD cues in isolation (Likova & Tyler, 2007).

Likova and Tyler identified an area anterior to hMT+ that seems particularly responsive to CD MID – the putative ‘cyclopean stereo motion’ area (Likova & Tyler, 2007; Figure 1.14). They used a random-dot CD stimulus containing no monocular motion cues. Responses to the CD stimulus were compared to responses to two different control stimuli – a static depth plane at zero disparity, and a disparity-matched control stimulus. This stimulus contained no coherent motion in depth but did contain static disparity over the same depth range as in their CD stimulus. Responses comparing the CD stimulus against either control stimulus were highly correlated. Thus, observed responses to the CD stimulus could not be accounted for by static disparity tuning. The authors suggest that disparity sensitive neurons identified in macaque MT may provide input to this anterior region for the processing of CD MID.

Figure 1.14 Responses to a CD motion stimulus, compared against a control stimulus. In this

example, the control stimulus consisted of a static depth plane at zero disparity. Responses are shown on an inflated brain (panel A) of an example subject, and on a flattened

representation showing the location of the peak activation (in the CSM ROI, dotted white line) relative to earlier visual areas. Note that the CSM is situated anterior to hMT+, and that there is no activation in hMT+ itself. In addition, there is a robust activation in the intraparietal parietal sulcus (IPS) but this is not discussed at length by the authors. Panel C shows the timecourse from within the hMT+ ROI and the CSM area during the CD stimulus condition. The CSM responds twice as strongly. Figure adapted from Likova & Tyler, 2007.

Rokers, Cormack and Huk also used fMRI to investigate the cortical locus of binocular MID processing (Rokers et al., 2009). Their paper outlined four separate experiments.

Experiment 1 used a mixed CD+IOVD stimulus to identify areas involved in MID processing. In experiments 2 and 3, they investigated the representation of CD and IOVD separately (see

Figure 1.15). Finally, an adaptation paradigm revealed areas showing directionally selective

response patterns to CD+IOVD cues. Their principal finding is that hMT+ is involved in the processing of all these stimulus types. In addition, their final experiment showed that, in hMT+, the fMRI signal was depressed when the test pattern was moving in the same

direction in depth as the adaptor. This adaptation effect suggests that hMT+ contains neurons tuned to a specific direction of MID.

42

Figure 1.15 fMRI responses measured across visual areas to CD (panel A) and IOVD (panel

B) stimuli. In panel A, the dark blue bar represents the response difference between a CD stimulus and a spatio-temporally scrambled (STS) control stimulus. Other bars show control conditions, where responses to spatially scrambled (SS) CD motion and temporally

scrambled (TS) CD motion were compared against the STS stimulus. The final comparison was between anti-correlated CD motion against an anti-correlated STS stimulus. In panel B, the dark blue bar shows the response to a motion through depth (MTD) stimulus where binocular dot pairs were correlated (containing both CD and IOVD). The light blue bar shows an anticorrelated version of the stimulus, which biases it towards IOVD motion. The motion within depth (MWD) conditions provide controls, where the same monocular motion energy is preserved but there is no MID signal to extract because binocular dot pairs are moving in the same direction. Error bars represent ±1 SEM. Figure adapted from Rokers et al., 2009.

There are some inconsistencies between the findings of these two papers. Likova and Tyler found no tuning to CD in hMT+. Instead, they identified CD responses in an adjacent, anterior area. Rokers, Cormack and Huk did not report results from this adjacent area, but did find CD tuning in hMT+. Differences in stimuli may have contributed to this – both groups used stimuli that were similar in MID speed, dot size and dot density, but the Rokers et al. stimulus was divided into four quadrants, where the MID trajectory was phase shifted by 180º in alternate quadrants. Thus, the stimulus contained both relative and absolute disparity cues. The Likova and Tyler stimulus consisted of a plane of dots oscillating in depth, thus

containing absolute disparity, but no relative disparity cues. Absolute and relative disparity appear to be processed via dissociable neural mechanisms, with absolute disparity engaging more dorsal visual areas (Neri, Bridge, & Heeger, 2004). There were also differences in the control stimulus that was used to subtract the signal from static disparity mechanisms – Rokers et al. used a control stimulus that was a non-structured cloud of dots containing a range of disparities, whereas Likova and Tyler used or a near or far disparity ‘surface’ of dots. These factors may contribute to the differences in cortical responses measured in these papers.

Joo et al. extended the findings from the fMRI-adaptation study described by Rokers et al., by measuring separate adaptation effects to CD and IOVD isolating stimuli. In hMT, the adaptation effect was stronger for IOVD than for CD stimuli, but no cross-cue adaptation effects were observed (Joo et al., 2016; see Figure 1.16). The adaptation effects in V1, V2, V3 and V3A were weak, suggesting that whilst these areas may provide inputs to hMT that are pertinent to the extraction of MID, they are unlikely to contain neurons tuned to 3D motion direction directly. In addition, the lack of cross-cue adaptation implies that whilst hMT

encodes both CD and IOVD-defined MID, different sub-populations of neurons in this area process either cue type. The authors suggest that this functional distinction may reflect the relative utility of CD and IOVD mechanisms for different perceptual tasks, consistent with the tuning properties of both cues (reviewed above in sections 1.4.6: Relative contributions of CD and IOVD to 3D motion processing, and 1.4.7: Spatiotemporal tuning of binocular MID

mechanisms).

Figure 1.16 Within-cue and cross-cue adaptation effects for MID stimuli. Panel A shows

within-cue adaptation for IOVD in orange, whilst cross-cue from CD to IOVD is shown in yellow. Panel B shows within-cue adaptation for CD in dark green, and cross-cue adaptation from IOVD to CD in light green. Effects were measured using fMRI across a range of visual areas. The adaptation index was calculated by normalising the difference between the

response amplitude to MID in the same direction between test and adapter, and the response amplitude to MID in the opposite direction between test and adapter, by its sum. Error bars indicate 68% confidence intervals. Figure adapted from Joo et al., 2016.