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Saccades during visual exploration align hippocampal 3-8 Hz rhythms in human and non-human primates.

Hoffman KL, Dragan MC, Leonard TK, Micheli C, Montefusco-Siegmund R, Valiante TA - Front Syst Neurosci (2013)

Bottom Line: The hippocampus, for example, shows oscillatory activity that is generally associated with encoding of information.The phase alignment depended on the task and not only on eye movements per se, and the frequency band was not a direct consequence of saccade rate.The present results may reflect a similar yet distinct primate homologue supporting active perception during exploration.

View Article: PubMed Central - PubMed

Affiliation: Department of Psychology, Centre for Vision Research, York University Toronto, ON, Canada ; Department of Biology, Centre for Vision Research, York University Toronto, ON, Canada ; Neuroscience Graduate Diploma Program, York University Toronto, ON, Canada.

ABSTRACT
Visual exploration in primates depends on saccadic eye movements (SEMs) that cause alternations of neural suppression and enhancement. This modulation extends beyond retinotopic areas, and is thought to facilitate perception; yet saccades may also influence brain regions critical for forming memories of these exploratory episodes. The hippocampus, for example, shows oscillatory activity that is generally associated with encoding of information. Whether or how hippocampal oscillations are influenced by eye movements is unknown. We recorded the neural activity in the human and macaque hippocampus during visual scene search. Across species, SEMs were associated with a time-limited alignment of a low-frequency (3-8 Hz) rhythm. The phase alignment depended on the task and not only on eye movements per se, and the frequency band was not a direct consequence of saccade rate. Hippocampal theta-frequency oscillations are produced by other mammals during repetitive exploratory behaviors, including whisking, sniffing, echolocation, and locomotion. The present results may reflect a similar yet distinct primate homologue supporting active perception during exploration.

No MeSH data available.


Related in: MedlinePlus

Localization of electrodes and evoked responses. (A) Renderings from patient 1's MR images with co-localized recording sites. On the left are two coronal sections showing the location of hippocampal depth macroelectrodes, with the most eccentric 1–2 contacts localized to the hippocampus, indicated by the blue dashes. On the right is a rendering of the whole brain, with the anterior tip oriented up and to the right, revealing the locations of subdural surface electrodes. This was the most common arrangement for the patients in this study. (B) Average evoked responses from several electrode locations, aligned to fixation onset. Time is on the x-axis, relative to fixation onset and magnitude in microvolts is on the Y axis. Time points of significant deviations are indicated by the lines at the bottom of the plot, color coded for the corresponding site (p < 0.001 cutoff of the fixation-time shuffled distribution). Note that the post-fixation response is qualitatively strongest in the hippocampus, and shows a polarity reversal across RHD sites; other locations such as the anterior temporal lobe show transient, broad-band modulation around the saccade event. For more information of the electrode locations sampled across subjects, see Table 1.
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Figure 2: Localization of electrodes and evoked responses. (A) Renderings from patient 1's MR images with co-localized recording sites. On the left are two coronal sections showing the location of hippocampal depth macroelectrodes, with the most eccentric 1–2 contacts localized to the hippocampus, indicated by the blue dashes. On the right is a rendering of the whole brain, with the anterior tip oriented up and to the right, revealing the locations of subdural surface electrodes. This was the most common arrangement for the patients in this study. (B) Average evoked responses from several electrode locations, aligned to fixation onset. Time is on the x-axis, relative to fixation onset and magnitude in microvolts is on the Y axis. Time points of significant deviations are indicated by the lines at the bottom of the plot, color coded for the corresponding site (p < 0.001 cutoff of the fixation-time shuffled distribution). Note that the post-fixation response is qualitatively strongest in the hippocampus, and shows a polarity reversal across RHD sites; other locations such as the anterior temporal lobe show transient, broad-band modulation around the saccade event. For more information of the electrode locations sampled across subjects, see Table 1.

Mentions: Fixation-aligned mean evoked responses (Figure 2) were considered significant if the mean observed response exceeded the 0.002 percentile of the mean shuffled-fixation response distribution (a two-sided test of the 1000-element distribution). Time-frequency plots aligned to fixation onset were calculated with FieldTrip using a Hanning window of 800 ms from −1.2 to 1.2 s (i.e., windows centered from −800 to 800 ms) taken every 10 ms, in 1-Hz increments from 3 to 80 Hz (Figures 3, 4) and from 3 to 20 Hz (Figure 5). The Hann (or Hanning) window was selected rather than multiple tapers to maximize temporal precision with minimal spectral leakage for these time-limited, low-frequency events of interest. Peri-fixational changes in power were tested by comparing an observed time-frequency power value to those of its fixation-time shuffled distribution, and FDR-correcting for the number of time-frequency points tested.


Saccades during visual exploration align hippocampal 3-8 Hz rhythms in human and non-human primates.

Hoffman KL, Dragan MC, Leonard TK, Micheli C, Montefusco-Siegmund R, Valiante TA - Front Syst Neurosci (2013)

Localization of electrodes and evoked responses. (A) Renderings from patient 1's MR images with co-localized recording sites. On the left are two coronal sections showing the location of hippocampal depth macroelectrodes, with the most eccentric 1–2 contacts localized to the hippocampus, indicated by the blue dashes. On the right is a rendering of the whole brain, with the anterior tip oriented up and to the right, revealing the locations of subdural surface electrodes. This was the most common arrangement for the patients in this study. (B) Average evoked responses from several electrode locations, aligned to fixation onset. Time is on the x-axis, relative to fixation onset and magnitude in microvolts is on the Y axis. Time points of significant deviations are indicated by the lines at the bottom of the plot, color coded for the corresponding site (p < 0.001 cutoff of the fixation-time shuffled distribution). Note that the post-fixation response is qualitatively strongest in the hippocampus, and shows a polarity reversal across RHD sites; other locations such as the anterior temporal lobe show transient, broad-band modulation around the saccade event. For more information of the electrode locations sampled across subjects, see Table 1.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3757337&req=5

Figure 2: Localization of electrodes and evoked responses. (A) Renderings from patient 1's MR images with co-localized recording sites. On the left are two coronal sections showing the location of hippocampal depth macroelectrodes, with the most eccentric 1–2 contacts localized to the hippocampus, indicated by the blue dashes. On the right is a rendering of the whole brain, with the anterior tip oriented up and to the right, revealing the locations of subdural surface electrodes. This was the most common arrangement for the patients in this study. (B) Average evoked responses from several electrode locations, aligned to fixation onset. Time is on the x-axis, relative to fixation onset and magnitude in microvolts is on the Y axis. Time points of significant deviations are indicated by the lines at the bottom of the plot, color coded for the corresponding site (p < 0.001 cutoff of the fixation-time shuffled distribution). Note that the post-fixation response is qualitatively strongest in the hippocampus, and shows a polarity reversal across RHD sites; other locations such as the anterior temporal lobe show transient, broad-band modulation around the saccade event. For more information of the electrode locations sampled across subjects, see Table 1.
Mentions: Fixation-aligned mean evoked responses (Figure 2) were considered significant if the mean observed response exceeded the 0.002 percentile of the mean shuffled-fixation response distribution (a two-sided test of the 1000-element distribution). Time-frequency plots aligned to fixation onset were calculated with FieldTrip using a Hanning window of 800 ms from −1.2 to 1.2 s (i.e., windows centered from −800 to 800 ms) taken every 10 ms, in 1-Hz increments from 3 to 80 Hz (Figures 3, 4) and from 3 to 20 Hz (Figure 5). The Hann (or Hanning) window was selected rather than multiple tapers to maximize temporal precision with minimal spectral leakage for these time-limited, low-frequency events of interest. Peri-fixational changes in power were tested by comparing an observed time-frequency power value to those of its fixation-time shuffled distribution, and FDR-correcting for the number of time-frequency points tested.

Bottom Line: The hippocampus, for example, shows oscillatory activity that is generally associated with encoding of information.The phase alignment depended on the task and not only on eye movements per se, and the frequency band was not a direct consequence of saccade rate.The present results may reflect a similar yet distinct primate homologue supporting active perception during exploration.

View Article: PubMed Central - PubMed

Affiliation: Department of Psychology, Centre for Vision Research, York University Toronto, ON, Canada ; Department of Biology, Centre for Vision Research, York University Toronto, ON, Canada ; Neuroscience Graduate Diploma Program, York University Toronto, ON, Canada.

ABSTRACT
Visual exploration in primates depends on saccadic eye movements (SEMs) that cause alternations of neural suppression and enhancement. This modulation extends beyond retinotopic areas, and is thought to facilitate perception; yet saccades may also influence brain regions critical for forming memories of these exploratory episodes. The hippocampus, for example, shows oscillatory activity that is generally associated with encoding of information. Whether or how hippocampal oscillations are influenced by eye movements is unknown. We recorded the neural activity in the human and macaque hippocampus during visual scene search. Across species, SEMs were associated with a time-limited alignment of a low-frequency (3-8 Hz) rhythm. The phase alignment depended on the task and not only on eye movements per se, and the frequency band was not a direct consequence of saccade rate. Hippocampal theta-frequency oscillations are produced by other mammals during repetitive exploratory behaviors, including whisking, sniffing, echolocation, and locomotion. The present results may reflect a similar yet distinct primate homologue supporting active perception during exploration.

No MeSH data available.


Related in: MedlinePlus