Limits...
A frontal cortex event-related potential driven by the basal forebrain.

Nguyen DP, Lin SC - Elife (2014)

Bottom Line: Event-related potentials (ERPs) are widely used in both healthy and neuropsychiatric conditions as physiological indices of cognitive functions.Contrary to the common belief that cognitive ERPs are generated by local activity within the cerebral cortex, here we show that an attention-related ERP in the frontal cortex is correlated with, and likely generated by, subcortical inputs from the basal forebrain (BF).These results highlight the important and previously unrecognized role of long-range subcortical inputs from the BF in the generation of cognitive ERPs.

View Article: PubMed Central - PubMed

Affiliation: Neural Circuits and Cognition Unit, Laboratory of Behavioral Neuroscience, National Institute on Aging, National Institutes of Health, Baltimore, United States.

ABSTRACT
Event-related potentials (ERPs) are widely used in both healthy and neuropsychiatric conditions as physiological indices of cognitive functions. Contrary to the common belief that cognitive ERPs are generated by local activity within the cerebral cortex, here we show that an attention-related ERP in the frontal cortex is correlated with, and likely generated by, subcortical inputs from the basal forebrain (BF). In rats performing an auditory oddball task, both the amplitude and timing of the frontal ERP were coupled with BF neuronal activity in single trials. The local field potentials (LFPs) associated with the frontal ERP, concentrated in deep cortical layers corresponding to the zone of BF input, were similarly coupled with BF activity and consistently triggered by BF electrical stimulation within 5-10 msec. These results highlight the important and previously unrecognized role of long-range subcortical inputs from the BF in the generation of cognitive ERPs. DOI: http://dx.doi.org/10.7554/eLife.02148.001.

Show MeSH
BF electrode locations and the classification of BF bursting neurons.(A) Each set of color boxes represent the locations of bilateral BF electrode bundle in one rat (n = 8). BF electrodes were located between −0.12 mm–−0.84 mm relative to Bregma throughout multiple subregions, including the ventral part of globus pallidus (GP), ventral pallidum (VP), substantia innominata (SI), nucleus basalis of Meynert (NBM, or B), magnocellular preoptic nucleus (MCPO) and horizontal limb of the diagonal band (HDB). This widespread spatial distribution of BF bursting neurons is consistent with the location of cortically-projecting BF neurons as revealed by placing retrograde tracers in the prefrontal cortex (Gritti et al., 1997). (B) PSTHs of all 168 BF neurons in response to oddball tone onset in hit trials. BF neurons were sorted by their bursting index, defined as the ratio of the bursting amplitude (average firing rate in the [50, 200] msec window) over the average firing rate in the entire session. Bursting index of 2.5 (indicated by the white dashed line) was used as the cutoff for classifying BF bursting neurons. (C) Scatter plot of the baseline firing rate vs bursting amplitude for all BF neurons. Each dot represents one BF neuron. The red dashed line indicates the 2.5 bursting index cutoff used for classifying BF bursting neurons.DOI:http://dx.doi.org/10.7554/eLife.02148.005
© Copyright Policy - open-access
Related In: Results  -  Collection

License
getmorefigures.php?uid=PMC3974155&req=5

fig1s2: BF electrode locations and the classification of BF bursting neurons.(A) Each set of color boxes represent the locations of bilateral BF electrode bundle in one rat (n = 8). BF electrodes were located between −0.12 mm–−0.84 mm relative to Bregma throughout multiple subregions, including the ventral part of globus pallidus (GP), ventral pallidum (VP), substantia innominata (SI), nucleus basalis of Meynert (NBM, or B), magnocellular preoptic nucleus (MCPO) and horizontal limb of the diagonal band (HDB). This widespread spatial distribution of BF bursting neurons is consistent with the location of cortically-projecting BF neurons as revealed by placing retrograde tracers in the prefrontal cortex (Gritti et al., 1997). (B) PSTHs of all 168 BF neurons in response to oddball tone onset in hit trials. BF neurons were sorted by their bursting index, defined as the ratio of the bursting amplitude (average firing rate in the [50, 200] msec window) over the average firing rate in the entire session. Bursting index of 2.5 (indicated by the white dashed line) was used as the cutoff for classifying BF bursting neurons. (C) Scatter plot of the baseline firing rate vs bursting amplitude for all BF neurons. Each dot represents one BF neuron. The red dashed line indicates the 2.5 bursting index cutoff used for classifying BF bursting neurons.DOI:http://dx.doi.org/10.7554/eLife.02148.005

Mentions: In 120 BF neurons recorded simultaneously with frontal EEG activity, 55% (66/120) showed robust bursting response to the oddball tone in hit trials and were classified as BF bursting neurons (Figure 1—figure supplement 2; Table 1). These BF neurons showed stronger bursting responses in hit trials than in miss trials, and in oddball trials than in standard trials (Figure 1F), consistent with the encoding of motivational salience as previously reported (Lin and Nicolelis, 2008; Avila and Lin, 2014). Interestingly, the timing of the BF bursting response as well as the modulation of BF bursting amplitude between different trial types (Figure 1F,G) were highly similar to those of the frontal ERP, suggesting that BF bursting may be functionally coupled with the frontal ERP.10.7554/eLife.02148.006Table 1.


A frontal cortex event-related potential driven by the basal forebrain.

Nguyen DP, Lin SC - Elife (2014)

BF electrode locations and the classification of BF bursting neurons.(A) Each set of color boxes represent the locations of bilateral BF electrode bundle in one rat (n = 8). BF electrodes were located between −0.12 mm–−0.84 mm relative to Bregma throughout multiple subregions, including the ventral part of globus pallidus (GP), ventral pallidum (VP), substantia innominata (SI), nucleus basalis of Meynert (NBM, or B), magnocellular preoptic nucleus (MCPO) and horizontal limb of the diagonal band (HDB). This widespread spatial distribution of BF bursting neurons is consistent with the location of cortically-projecting BF neurons as revealed by placing retrograde tracers in the prefrontal cortex (Gritti et al., 1997). (B) PSTHs of all 168 BF neurons in response to oddball tone onset in hit trials. BF neurons were sorted by their bursting index, defined as the ratio of the bursting amplitude (average firing rate in the [50, 200] msec window) over the average firing rate in the entire session. Bursting index of 2.5 (indicated by the white dashed line) was used as the cutoff for classifying BF bursting neurons. (C) Scatter plot of the baseline firing rate vs bursting amplitude for all BF neurons. Each dot represents one BF neuron. The red dashed line indicates the 2.5 bursting index cutoff used for classifying BF bursting neurons.DOI:http://dx.doi.org/10.7554/eLife.02148.005
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3974155&req=5

fig1s2: BF electrode locations and the classification of BF bursting neurons.(A) Each set of color boxes represent the locations of bilateral BF electrode bundle in one rat (n = 8). BF electrodes were located between −0.12 mm–−0.84 mm relative to Bregma throughout multiple subregions, including the ventral part of globus pallidus (GP), ventral pallidum (VP), substantia innominata (SI), nucleus basalis of Meynert (NBM, or B), magnocellular preoptic nucleus (MCPO) and horizontal limb of the diagonal band (HDB). This widespread spatial distribution of BF bursting neurons is consistent with the location of cortically-projecting BF neurons as revealed by placing retrograde tracers in the prefrontal cortex (Gritti et al., 1997). (B) PSTHs of all 168 BF neurons in response to oddball tone onset in hit trials. BF neurons were sorted by their bursting index, defined as the ratio of the bursting amplitude (average firing rate in the [50, 200] msec window) over the average firing rate in the entire session. Bursting index of 2.5 (indicated by the white dashed line) was used as the cutoff for classifying BF bursting neurons. (C) Scatter plot of the baseline firing rate vs bursting amplitude for all BF neurons. Each dot represents one BF neuron. The red dashed line indicates the 2.5 bursting index cutoff used for classifying BF bursting neurons.DOI:http://dx.doi.org/10.7554/eLife.02148.005
Mentions: In 120 BF neurons recorded simultaneously with frontal EEG activity, 55% (66/120) showed robust bursting response to the oddball tone in hit trials and were classified as BF bursting neurons (Figure 1—figure supplement 2; Table 1). These BF neurons showed stronger bursting responses in hit trials than in miss trials, and in oddball trials than in standard trials (Figure 1F), consistent with the encoding of motivational salience as previously reported (Lin and Nicolelis, 2008; Avila and Lin, 2014). Interestingly, the timing of the BF bursting response as well as the modulation of BF bursting amplitude between different trial types (Figure 1F,G) were highly similar to those of the frontal ERP, suggesting that BF bursting may be functionally coupled with the frontal ERP.10.7554/eLife.02148.006Table 1.

Bottom Line: Event-related potentials (ERPs) are widely used in both healthy and neuropsychiatric conditions as physiological indices of cognitive functions.Contrary to the common belief that cognitive ERPs are generated by local activity within the cerebral cortex, here we show that an attention-related ERP in the frontal cortex is correlated with, and likely generated by, subcortical inputs from the basal forebrain (BF).These results highlight the important and previously unrecognized role of long-range subcortical inputs from the BF in the generation of cognitive ERPs.

View Article: PubMed Central - PubMed

Affiliation: Neural Circuits and Cognition Unit, Laboratory of Behavioral Neuroscience, National Institute on Aging, National Institutes of Health, Baltimore, United States.

ABSTRACT
Event-related potentials (ERPs) are widely used in both healthy and neuropsychiatric conditions as physiological indices of cognitive functions. Contrary to the common belief that cognitive ERPs are generated by local activity within the cerebral cortex, here we show that an attention-related ERP in the frontal cortex is correlated with, and likely generated by, subcortical inputs from the basal forebrain (BF). In rats performing an auditory oddball task, both the amplitude and timing of the frontal ERP were coupled with BF neuronal activity in single trials. The local field potentials (LFPs) associated with the frontal ERP, concentrated in deep cortical layers corresponding to the zone of BF input, were similarly coupled with BF activity and consistently triggered by BF electrical stimulation within 5-10 msec. These results highlight the important and previously unrecognized role of long-range subcortical inputs from the BF in the generation of cognitive ERPs. DOI: http://dx.doi.org/10.7554/eLife.02148.001.

Show MeSH