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Deviance detection by a P3-like response in rat posterior parietal cortex.

Imada A, Morris A, Wiest MC - Front Integr Neurosci (2013)

Bottom Line: Extending previous results from surface recordings we found, after controlling for the frequencies of the standard and oddball tones, that rat frontal and parietal-evoked LFPs (eLFPs) exhibit significantly larger N1 (~40 ms latency), P2 (~100 ms), N2 (~160 ms), P3E (~200-240 ms), and P3L (~300-500 ms) amplitudes after an oddball tone.We compared the difference between rare-tone and frequent-tone response amplitudes in the two-tone context (oddball effect) or single-tone context which isolates the contribution of SSA (SSA effect).An analysis of variance (ANOVA) revealed a significant main effect of tone context on rare-tone response enhancements, showing that the rare-tone enhancements were stronger in the two-tone context than the single-tone context.

View Article: PubMed Central - PubMed

Affiliation: Neuroscience Program, Wellesley College Wellesley, MA, USA.

ABSTRACT
To better understand sensory processing in frontal and parietal cortex of the rat, and to further assess the rat as a model of human frontal-parietal processing, we recorded local field potentials (LFPs) from microelectrode arrays implanted in medio-dorsal frontal, and posterior parietal cortex of awake rats as they were presented with a succession of frequent "standard" tones and infrequent "oddball" tones. Extending previous results from surface recordings we found, after controlling for the frequencies of the standard and oddball tones, that rat frontal and parietal-evoked LFPs (eLFPs) exhibit significantly larger N1 (~40 ms latency), P2 (~100 ms), N2 (~160 ms), P3E (~200-240 ms), and P3L (~300-500 ms) amplitudes after an oddball tone. These neural oddball effects could contribute to the automatic allocation of attention to rare stimuli. To determine whether these enhanced responses to rare stimuli could be accounted for in terms of stimulus-specific neural adaptation (SSA), we also recorded during single-tone control sessions involving frequent standard, or infrequent oddball beeps alone. We compared the difference between rare-tone and frequent-tone response amplitudes in the two-tone context (oddball effect) or single-tone context which isolates the contribution of SSA (SSA effect). An analysis of variance (ANOVA) revealed a significant main effect of tone context on rare-tone response enhancements, showing that the rare-tone enhancements were stronger in the two-tone context than the single-tone context. This difference between tone contexts was greatest at the early P3E peak (200-240 ms post-beep) in parietal cortex, suggesting true deviance detection by this evoked response component, which cannot be accounted for in terms of simple models of SSA.

No MeSH data available.


Auditory eLFPs recorded during two example pairs of two-tone oddball sessions. (A)Top left panel—eLFPs recorded in parietal cortex of one rat while the high-pitched tone was presented rarely as oddball (red) and the low-pitched tone was presented frequently as standard (blue). The five eLFP peaks that we studied are labeled: N1 (~40 ms), P2 (~100 ms), N2 (~160 ms), an early P3E (~250 ms), and a late P3L (>300 ms). Bottom left panel—eLFPs recorded from the same frontal electrode in the same rat as in the top left panel, in a separate session with pitches reversed: the high-pitched tone was presented as standard (blue) and the low-pitched tone was presented as oddball (red). Top right panel—Comparing oddball and standard response amplitudes from a single two-tone session confounds frequency-dependent responding with any potential enhanced responses to rare stimuli. Therefore, we compare responses to the high-pitched tone presented as oddball (red), with responses to the same high-pitched tone presented as standard (blue) in a matched session in the same animal. Bottom right panel—shows the difference between the oddball and standard eLFPs from the top right panel, with a 68% confidence interval based on the variability across trials. The positive difference around 250 ms post-stimulus corresponds to an enhanced parietal P3E amplitude in response to the rare oddball tone. (B) Shows eLFPs recorded in frontal cortex of a different rat than (A), during a high-pitched oddball session (top left panel ofB), a low-pitched oddball session (bottom left panel), a comparison of the high-pitched oddball eLFP with the high-pitched standard eLFP (top right panel ofB), and the difference curve with 68% confidence interval (bottom right panel). In this pair of sessions the rare-tone response was amplified at the N1, P2, N2, and P3L peaks.
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Figure 1: Auditory eLFPs recorded during two example pairs of two-tone oddball sessions. (A)Top left panel—eLFPs recorded in parietal cortex of one rat while the high-pitched tone was presented rarely as oddball (red) and the low-pitched tone was presented frequently as standard (blue). The five eLFP peaks that we studied are labeled: N1 (~40 ms), P2 (~100 ms), N2 (~160 ms), an early P3E (~250 ms), and a late P3L (>300 ms). Bottom left panel—eLFPs recorded from the same frontal electrode in the same rat as in the top left panel, in a separate session with pitches reversed: the high-pitched tone was presented as standard (blue) and the low-pitched tone was presented as oddball (red). Top right panel—Comparing oddball and standard response amplitudes from a single two-tone session confounds frequency-dependent responding with any potential enhanced responses to rare stimuli. Therefore, we compare responses to the high-pitched tone presented as oddball (red), with responses to the same high-pitched tone presented as standard (blue) in a matched session in the same animal. Bottom right panel—shows the difference between the oddball and standard eLFPs from the top right panel, with a 68% confidence interval based on the variability across trials. The positive difference around 250 ms post-stimulus corresponds to an enhanced parietal P3E amplitude in response to the rare oddball tone. (B) Shows eLFPs recorded in frontal cortex of a different rat than (A), during a high-pitched oddball session (top left panel ofB), a low-pitched oddball session (bottom left panel), a comparison of the high-pitched oddball eLFP with the high-pitched standard eLFP (top right panel ofB), and the difference curve with 68% confidence interval (bottom right panel). In this pair of sessions the rare-tone response was amplified at the N1, P2, N2, and P3L peaks.

Mentions: We first wanted to assess the extent to which the responses to rare-tones were enhanced at our frontal and parietal recording sites. Figure 1 shows eLFPs from two example pairs of sessions in different rats. The peaks labeled in the top left panel of Figure 1A define our nomenclature for the components of the eLFPs we studied (see “Materials and Methods”): N1 at a latency of about 40 ms, P2 near 100 ms, and an “early” P3E around 200–250 ms. We also examined an N2 component between the P2 and P3E peaks, although in this session the minimum potentials in that time window were barely negative. We also considered a “late” P3L peak after 300 ms latency, which in this session appeared at different latencies in the two-tone conditions (oddball and standard). The example in Figure 1A shows eLFPs recorded in parietal cortex. In the pair of sessions illustrated in Figure 1A, the response to the rare oddball stimulus was larger in amplitude than the response to the frequent standard tone, regardless of whether the oddball was the higher-pitched (top left of Figure 1A) or the lower-pitched tone (bottom left of Figure 1A). Nevertheless, since we are interested in the differential response to rare and frequent tones, rather than different obligatory responses to different pitches, the meaningful comparison is between the high-pitch oddball eLFP and the high-pitch standard eLFP (top right of Figure 1A). In this example pair of sessions, the rare-tone response enhancement is strongest at the early P3E peak.


Deviance detection by a P3-like response in rat posterior parietal cortex.

Imada A, Morris A, Wiest MC - Front Integr Neurosci (2013)

Auditory eLFPs recorded during two example pairs of two-tone oddball sessions. (A)Top left panel—eLFPs recorded in parietal cortex of one rat while the high-pitched tone was presented rarely as oddball (red) and the low-pitched tone was presented frequently as standard (blue). The five eLFP peaks that we studied are labeled: N1 (~40 ms), P2 (~100 ms), N2 (~160 ms), an early P3E (~250 ms), and a late P3L (>300 ms). Bottom left panel—eLFPs recorded from the same frontal electrode in the same rat as in the top left panel, in a separate session with pitches reversed: the high-pitched tone was presented as standard (blue) and the low-pitched tone was presented as oddball (red). Top right panel—Comparing oddball and standard response amplitudes from a single two-tone session confounds frequency-dependent responding with any potential enhanced responses to rare stimuli. Therefore, we compare responses to the high-pitched tone presented as oddball (red), with responses to the same high-pitched tone presented as standard (blue) in a matched session in the same animal. Bottom right panel—shows the difference between the oddball and standard eLFPs from the top right panel, with a 68% confidence interval based on the variability across trials. The positive difference around 250 ms post-stimulus corresponds to an enhanced parietal P3E amplitude in response to the rare oddball tone. (B) Shows eLFPs recorded in frontal cortex of a different rat than (A), during a high-pitched oddball session (top left panel ofB), a low-pitched oddball session (bottom left panel), a comparison of the high-pitched oddball eLFP with the high-pitched standard eLFP (top right panel ofB), and the difference curve with 68% confidence interval (bottom right panel). In this pair of sessions the rare-tone response was amplified at the N1, P2, N2, and P3L peaks.
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Related In: Results  -  Collection

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Figure 1: Auditory eLFPs recorded during two example pairs of two-tone oddball sessions. (A)Top left panel—eLFPs recorded in parietal cortex of one rat while the high-pitched tone was presented rarely as oddball (red) and the low-pitched tone was presented frequently as standard (blue). The five eLFP peaks that we studied are labeled: N1 (~40 ms), P2 (~100 ms), N2 (~160 ms), an early P3E (~250 ms), and a late P3L (>300 ms). Bottom left panel—eLFPs recorded from the same frontal electrode in the same rat as in the top left panel, in a separate session with pitches reversed: the high-pitched tone was presented as standard (blue) and the low-pitched tone was presented as oddball (red). Top right panel—Comparing oddball and standard response amplitudes from a single two-tone session confounds frequency-dependent responding with any potential enhanced responses to rare stimuli. Therefore, we compare responses to the high-pitched tone presented as oddball (red), with responses to the same high-pitched tone presented as standard (blue) in a matched session in the same animal. Bottom right panel—shows the difference between the oddball and standard eLFPs from the top right panel, with a 68% confidence interval based on the variability across trials. The positive difference around 250 ms post-stimulus corresponds to an enhanced parietal P3E amplitude in response to the rare oddball tone. (B) Shows eLFPs recorded in frontal cortex of a different rat than (A), during a high-pitched oddball session (top left panel ofB), a low-pitched oddball session (bottom left panel), a comparison of the high-pitched oddball eLFP with the high-pitched standard eLFP (top right panel ofB), and the difference curve with 68% confidence interval (bottom right panel). In this pair of sessions the rare-tone response was amplified at the N1, P2, N2, and P3L peaks.
Mentions: We first wanted to assess the extent to which the responses to rare-tones were enhanced at our frontal and parietal recording sites. Figure 1 shows eLFPs from two example pairs of sessions in different rats. The peaks labeled in the top left panel of Figure 1A define our nomenclature for the components of the eLFPs we studied (see “Materials and Methods”): N1 at a latency of about 40 ms, P2 near 100 ms, and an “early” P3E around 200–250 ms. We also examined an N2 component between the P2 and P3E peaks, although in this session the minimum potentials in that time window were barely negative. We also considered a “late” P3L peak after 300 ms latency, which in this session appeared at different latencies in the two-tone conditions (oddball and standard). The example in Figure 1A shows eLFPs recorded in parietal cortex. In the pair of sessions illustrated in Figure 1A, the response to the rare oddball stimulus was larger in amplitude than the response to the frequent standard tone, regardless of whether the oddball was the higher-pitched (top left of Figure 1A) or the lower-pitched tone (bottom left of Figure 1A). Nevertheless, since we are interested in the differential response to rare and frequent tones, rather than different obligatory responses to different pitches, the meaningful comparison is between the high-pitch oddball eLFP and the high-pitch standard eLFP (top right of Figure 1A). In this example pair of sessions, the rare-tone response enhancement is strongest at the early P3E peak.

Bottom Line: Extending previous results from surface recordings we found, after controlling for the frequencies of the standard and oddball tones, that rat frontal and parietal-evoked LFPs (eLFPs) exhibit significantly larger N1 (~40 ms latency), P2 (~100 ms), N2 (~160 ms), P3E (~200-240 ms), and P3L (~300-500 ms) amplitudes after an oddball tone.We compared the difference between rare-tone and frequent-tone response amplitudes in the two-tone context (oddball effect) or single-tone context which isolates the contribution of SSA (SSA effect).An analysis of variance (ANOVA) revealed a significant main effect of tone context on rare-tone response enhancements, showing that the rare-tone enhancements were stronger in the two-tone context than the single-tone context.

View Article: PubMed Central - PubMed

Affiliation: Neuroscience Program, Wellesley College Wellesley, MA, USA.

ABSTRACT
To better understand sensory processing in frontal and parietal cortex of the rat, and to further assess the rat as a model of human frontal-parietal processing, we recorded local field potentials (LFPs) from microelectrode arrays implanted in medio-dorsal frontal, and posterior parietal cortex of awake rats as they were presented with a succession of frequent "standard" tones and infrequent "oddball" tones. Extending previous results from surface recordings we found, after controlling for the frequencies of the standard and oddball tones, that rat frontal and parietal-evoked LFPs (eLFPs) exhibit significantly larger N1 (~40 ms latency), P2 (~100 ms), N2 (~160 ms), P3E (~200-240 ms), and P3L (~300-500 ms) amplitudes after an oddball tone. These neural oddball effects could contribute to the automatic allocation of attention to rare stimuli. To determine whether these enhanced responses to rare stimuli could be accounted for in terms of stimulus-specific neural adaptation (SSA), we also recorded during single-tone control sessions involving frequent standard, or infrequent oddball beeps alone. We compared the difference between rare-tone and frequent-tone response amplitudes in the two-tone context (oddball effect) or single-tone context which isolates the contribution of SSA (SSA effect). An analysis of variance (ANOVA) revealed a significant main effect of tone context on rare-tone response enhancements, showing that the rare-tone enhancements were stronger in the two-tone context than the single-tone context. This difference between tone contexts was greatest at the early P3E peak (200-240 ms post-beep) in parietal cortex, suggesting true deviance detection by this evoked response component, which cannot be accounted for in terms of simple models of SSA.

No MeSH data available.