Differences between the single cell activity in rostral and caudal subregions of PMd during complex visuomotor control

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 Such 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 2,3,4 lobe (SPL) and dorsal premotor cortex (PMd) . Here we further examine the role of the premotor cortex in this behaviour. More specifically we were interested in exploring the possible changes in neuronal activity between PMdr and PMdc when the eyes and hand were decoupled. Similar to our previously reported LFP results, we observed distinct task-related differences as well as topographical differences between the single cell activity and spike-field coherency of PMdr and PMdc. These data further characterize the nature of visuomotor transformations within these regions during non-standard reach.
A
LF CS AS

Neurophysiology Results
Topographical and task related differences in LFPs:
A
16 14 12 10 8 6 4 2 0 -2 -4 -.5

Task related differences in cell discharge rates:

A
Normalized firing rate (Hz)
35 30 25 20 15 10 5 0 -5 -10 -15 -.5

Normalized power

Normalized power

***

****

0.5

1 -.5

0.5

16 14 12 10 8 6 4 2 0 -2 -4 -.5

Normalized firing rate (Hz)

IDP

PMdr

B
MOVE IDP

PMdc

MOVE

IDP

PMdr

B
MOVE
10 5 0 -5 0.5 35 30 25 20 15 10 5 0 -5 -10 -15 -.5

IDP

PMdc

MOVE
10 5 0 -5 0.5

0.5

1 -.5

0.5

0.5

1 -.5

0.5

1 -.5

Time(sec)

Time(sec)

Time(sec)

Time(sec)

Figure 3. Line plots demonstrating task related difference during the IDP (left panels) and MOVE (right panels) epochs. Z scores represent the overall power across frequency (0-70Hz) over time. Astericks denotes significantly difference between condition (P < 0.05, jacknife error bars).

Figure 4. Mean discharge rates of single cells within PMd across the tasks. A, Mean normalized firing rates for PMdr during standard and non-standard condition. B, Mean normalized firing rates for PMdc during standard and non-standard conditions. Black lines represent peripheral cue onset during the IDP epoch (left panels) and movement onset during the MOVE epoch (right panels), jacknife error bars.

Topographical differences in cell discharge rates:

Normalized firing rate (Hz) Normalized firing rate (Hz)

A IDP Period ** 25 ** **
20 15 10 5 0 -5 PMdc PMdr

B
6 4 2 0 -2 -4

PMdc

MOVE Period ** PMdr **

**

**

Figure 5. Histogram demonstrating significant differences in the normalized mean firing rates between PMdr and PMdc. A, Normalized firing rates as a function of condition and location during the IDP epoch. B, Normalized firing rates during MOVE epoch broken up into early (before movement onset) and late (after movement onset) periods. Significant difference between either conditions or locations are represented by asterisks (* P <0.05, ** P <0.01).

B
AS

LF CS

Figure 1: Penetration sites for monkey A (A) and monkey B (B). Larger dots indicate where recordings were obtained on two occasions. AS: arcuate sulcus. CS: central sulcus. LF: Longitudinal fissure.Dotted line denotes division between penetration sites classified as rostral (left of line) or caudal (right of line). A
70 60 50 40 30 20 10 0 -.5

Early

Late

Early

Late

Location

Epoch

Spike-field coherence is stronger in PMdr:

0.15
0

Normalized z score

Standard condition

Non-standard condition
Eye and hand decoupled Figure 2: Experimental setup and trial timing. Visual presentation of the task was either over a horizontal touch sensitive monitor (A, standard condition) or on a vertical monitor (B, Nonstandard condition). 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.

Eye and hand congruent

Frequency (Hz)

Frequency (Hz)

Methods

PMdr
IDP

B Standard
MOVE
70 60 50 40 30 20 10 0 -.5

A
2 1 0 -1 -2 -3 -4 -5 -6 -7 -.5

Non-standard
IDP MOVE

IDP

PMdr

MOVE

***

**** ***

Time(sec)

.5

1 -.5

Time(sec)

.5

Time(sec)

.5

1 -.5

Time(sec)

.5

0.5

1 -.5

8 6 4 2 0 -2 -4 -6 -8 0.5

Standard Non-standard

C PMdc
70 60 50 40 30 20 10 0 -.5

Frequency (Hz)

Frequency (Hz)

MT RT IDP 2000 500 ms CHT 500 ms

MT RT IDP 2000 500 ms CHT 500 ms

Time(sec)

.5

1 -.5

Time(sec)

.5

Time(sec)

.5

1 -.5

Time(sec)

.5

Normalized z score

THT 500 ms

THT 500 ms

IDP

Standard

D
70 60 50 40 30 20 10 0 -.5

Time(sec)

Non-standard
IDP MOVE

B
2 1 0 -1 -2 -3 -4 -5 -6 -7 -.5

MOVE

IDP

PMdc

MOVE

0.5

1 -.5

8 6 4 2 0 -2 -4 -6 -8 0.5

Normalized z score

Normalized z score

Monkeys (2 female macaca mulatta) were trained to perform centre out reaching tasks. Each trial began with the appearance of a centre target. Once the animal fixated and held their hand at this target one of eight equally spaced (45) peripheral targets were presented. After a variable cue period the animal received a go signal to move their hand AND eye towards the peripheral target. Arm movements were always made over the horizontal touch screen. However the visual presentation was either over a horizontal touch sensitive monitor (A, standard condition) or on a vertical monitor (B, Non-standard condition). 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. We examined the single unit and oscillatory activity within PMdr and PMdc during standard and non-standard situations (Figure 2). The full trajectory of the hand and eye were recorded to ensure that the motor task remained similar between conditions. 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.

Figure 6. Population spike-field coherency demonstrating topographical differences between PMdr (A,B) and PMdc (C,D). Standard conditions are on the left (A,C) and non-standard conditions are on the right (B,C). Black line indicates peripheral target onset during IDP epochs and movement onset during MOVE epochs, gray dashed line indicates end of the baseline period. Power is color-coded on a log scale.

Time(sec)

Figure 7. Population averaged 30-45Hz spike-field coherence within PMdr (A) and PMdc (B) across time. Asterisks denote significant difference between condition (P < 0.05, jacknife error bars).

PMdr spike-field coherence increases within the gamma range:

A
2 1 0 -1 -2 -3 -4 -5 -6 -7

B
IDP
4 2 0 -2 -4 -6 -8 0 10 20 30 40 50 60 70

MOVE

**** *

*********

PMdr, Standard PMdr, Non-standard PMdc, Standard PMdc, Non-standard

Figure 8. Spike-field coherence line plot for IDP (A) and MOVE (B) epochs. PMdr in black and PMdc in grey. Coherence is z-transformed. Asterisks denote significant difference between conditions within each region (P < 0.05, jacknife error bars).
Frequency (Hz)

0 10 20 30 40 50 60 70

Frequency (Hz)

Conclusions
Activity in PMdr and PMdc are modulated by a decoupled versus a coupled reach.
-This suggests that both regions within PMd are involved in non-standard reaching.

These differences are topographical, PMdr is more active than PMdc during decoupled reaching. Spike-field coherency was greater within PMdr during decoupled reaching.
-Spike-field coherence is thought to reflect the contributions of neurons to the local processing, or computations within a region. These data supports the idea that PMdr is a crucial region in the integration of the implicit rule about the relationship between vision and proprioception 1. Wise et al., (1996) Can. J. Physiol. Pharmacol. 74: 469482. required for complex decoupled reaching. 2. Diana et al., (2004) NeuroIm. 23: 1100-1111.
3. Hawkins et al., (2013) J. of Cog. Neurosci. 25:436-454. 4. Sayegh et al., (in review) J. of Neurophys.