LFP activity within PMd and SPL during decoupled visually-guided reaching

P. F. Sayegh, K. M. Hawkins & L. E. Sergio . ` School of Kinesiology and Health Science, Centre for Vision Research, York University, Toronto, Ontario, Canada.

Introduction
The objective of our research is to understand how the brain plans and executes visually-guided reaching movements when the motions of the eye and hand are decoupled. These decoupled movements are referred to as 'non-standard' movements and rely on the integration of specific cognitive 1. rules into the motor plan These movements differ from 'standard' movements in which the visual object is the target of 1. the action Our previous research has demonstrated that these non-standard movements are associated with activity in a network of brain regions that includes the superior parietal lobe 2,3,4 (SPL) and dorsal premotor cortex (PMd) . Here we examined the contribution of the local cell assemblies in PMd and SPL during non-standard reaching movements. We observed distinct functional differences between SPL, PMdr and PMdc. Specifically, oscillatory activity within PMdr was enhanced during non-standard conditions along with a sharpening in directional tuning. SPL and PMdc showed decreased activity during non-standard conditions and a loss of directional tuning. Taken collectively, these results support separate roles for these region in visuomotor transformation.
Figure 1: Cortical regions accessed by chamber placement: The black circle represents location of PMd chamber and the gray circle represents location of SPL chamber Adapted from Kalaska et. al., Curr. Op. Neurobiol. 1997. 100 0

Behavioural Results
Percent of pop.

Topographical changes in directional tuning during decoupled reaching

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Tuned Lost tuning with decoupling Tuned for both tasks

Similar hand trajectories between conditions:

Monkey A Standard Monkey A Non-Standard 100 0 Monkey B Standard 100 Monkey B Non-Standard 100 0

Figure 5: Histograms of directional tuning within PMd and SPL: Some sites demonstrate directional tuning during either condition, some sites lost tuning during the decoupled condition and some sites were directionally tuned for both conditions.

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Figure 3: Mean reach trajectories. Black lines: mean movement trajectories, black tick marks: standard deviations. Yellow asterisks denote trajectory segments that were significantly (p < .05) more variable in comparison to the standard condition.

Maintained tuning Rotated

Neurophysiological Results
Topographical difference between regions during decoupled reaching: 10 5 0 -5 -10
PMdr A
100 Hz

Figure 6: Histograms of sub-population of sites within PMd and SPL that were directionally tuned during both conditions: Sub-population of sites that were directionally tuned during both conditions. Of these sites, some maintained tuning between conditions, while other sites showed a rotation in preferred direction when the eye from the hand were decoupled.

PMdr PMdc SPL

Sharpening and rotation in PD within PMdr during decoupled reach

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Methods
A Standard condition
Eye and hand congruent

Non-standard condition
Eye and hand decoupled

Figure 4: Population time-frequency spectrograms of PMd and SPL activity during the IDP periods: Spectrograms on left side for each condition show IDP period and are aligned to the peripheral target onset. A) Population spectrograms of PMdr activity. B) Population spectrograms of PMdc activity. C) Population spectrograms of SPL activity. Black line indicates peripheral target onset, gray dashed line indicates end of the baseline period.

Figure 7: Population directional tuning during IDP period for PMd and SPL: Population polar plots demonstrate the sharpening of directional tuning as well as the magnitude of any rotation that occurs between conditions. Black line represents standard condition, red line represents non-standard condition.

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Eye fixation, central target

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Figure 2: Experimental setup and trial timing. A) Schematic of the standard and dissociated conditions. B) During each trial, one of eight equally spaced (45) peripheral targets were presented on either a touch-sensitive screen placed over the animals lap or on a monitor positioned vertically 40 cm away from the animals frontal plane. Arm movements were always made over the horizontal touch screen. Light grey circles represent the eight possible target locations (not illuminated before cue). Epochs - CHT: centre hold time, IDP: instructed delay period, RT: reaction time, MT: movement time, THT: target hold time. Red horizontal line represents the time in which the animal had to maintain fixation and hand inside the central target. The animal's head was fixed throughout the experiment.

Time (msec) Time (msec) 10 5 0 -5 -10

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Figure 4: Population early IDP spectrograms for PMd and SPL activity during standard and nonstandard conditions: Spectrograms on left side show activity during standard conditions, spectrograms on right side show activity during non-standard conditions. A) Beta oscillatory activity. PMdr shows stronger beta activity specifically during the non-standard condition. B) Low gamma oscillatory activity. PMdr shows the strongest low gamma activity overall with the strongest activity during the non-standard condition. C) Gamma oscillatory activity. Time zero represents peripheral target onset. PMdr shows the strongest gamma activity during both conditions with the strongest activity during the non-standard condition.

Conclusions
PMdr and decoupled reaches:
-Enhanced oscillatory activity during decoupled reach likely reflects the additional cognitive processing needed to integrate the new transformational rule into the motor plan. -Sharpening and rotation of PD during decoupled reach may reflect the incongruence between proprioception signal from the hand and visual signal from the cursor (representing the hand location) on the vertical monitor.

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We examined eye and hand movement related LFP activity within PMd and SPL during standard and non-standard situations (Figure 2). Monkeys (2 female macaca mulatta) were trained to fixate on a central target throughout the instructed delay period, then to move their eyes and hand to one of eight peripherally cued targets and hold them there throughout the target hold period. The full trajectory of the hand and eye were recorded to ensure that the motor task remained similar between conditions. Eye movements were monitored using the ISCAN-ETL 200 Eye Tracking System (ISCAN Inc, Burlington MA) at a sampling rate of 1KHz. Hand paths were monitored using a touch sensitive screen (100Hz, Touch Controls Inc, San Diego CA). A four electrode microdrive (FHC Inc.) was used in conjunction with a multi-unit recording system (Alpha-Omega Engineering, Israel) to collect single unit (12.5kHz) and waveform (1562.5 Hz) activity. Data were analyzed in Matlab (Mathworks, USA) using both custom written and open source (Chronux.org) programmes.

Oscillatory activity modulated by gaze effects:

REGION
PMdr PMdc SPL
0 - 10Hz 0.068 0.17 0.12 10 - 20Hz 20 - 30Hz 30 - 40Hz 40 - 50Hz 50 - 60Hz 60 - 70Hz 70 - 80Hz 80 - 90Hz 90 - 100Hz 0.66 0.15 0.25 0.89 0.95 0.33 0.81 0.37 0.45 0.22 0.21 0.56 0.56 0.20 0.35 0.11 0.32 0.05 0.04* 0.10 0.04* 0.02* 0.30 0.05 0.02* 0.76 0.02*

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PMdc and SPL and decoupled reaches:

-The decreased oscillatory activity during decoupled reach suggests that these regions may not be critical for non-standard movements. -The decrease in the strength of tuning also supports this conclusion.
References: 1. Wise et al (1996) Can J Physiol Pharmacol 74:469482. 2. Gorbet et. al. (2004) Neuroimage, 23: 1100-1111. 3. Granek et. al. (2010) Cortex, 46(9): 1165-1177. 4. Sayegh et. al. (2009) SFN 455.0 5. Pesaren et. al. (2008) Nature, 453: 406-409.

Table 1: Differences in Oscillatory activity with changes in gaze angle: P-values for comparisons between eye control conditions. Eye control conditions were performed on the horizontal touch screen and vertical monitor. These conditions required the animal to fixate on targets located in the same location as those from experimental conditions. No reach movement was performed. These eye control conditions served to analyse if oscillatory activity within each region was affected by just gaze angle for a given plane. Asterisks denotes significant difference in oscillatory activity from the overall change in gaze angle that occurs between standard and non-standard conditions.