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Human Temporal Cortical Single Neuron Activity during Language: A Review.

Ojemann GA - Brain Sci (2013)

Bottom Line: The majority of the changes in activity were tonic sustained shifts in firing.Patterned phasic activity for specific language items was very infrequently recorded.Human single neuron recordings provide a unique perspective on the biologic substrate for language, for these findings are in contrast to many of the findings from other techniques for investigating this.

View Article: PubMed Central - PubMed

Affiliation: Department of Neurological Surgery, University of Washington, Box 356470, Seattle, WA 98195, USA. gojemann@u.washington.edu.

ABSTRACT
Findings from recordings of human temporal cortical single neuron activity during several measures of language, including object naming and word reading are reviewed and related to changes in activity in the same neurons during recent verbal memory and verbal associative learning measures, in studies conducted during awake neurosurgery for the treatment of epilepsy. The proportion of neurons changing activity with language tasks was similar in either hemisphere. Dominant hemisphere activity was characterized by relative inhibition, some of which occurred during overt speech, possibly to block perception of one's own voice. However, the majority seems to represent a dynamic network becoming active with verbal memory encoding and especially verbal learning, but inhibited during performance of overlearned language tasks. Individual neurons are involved in different networks for different aspects of language, including naming or reading and naming in different languages. The majority of the changes in activity were tonic sustained shifts in firing. Patterned phasic activity for specific language items was very infrequently recorded. Human single neuron recordings provide a unique perspective on the biologic substrate for language, for these findings are in contrast to many of the findings from other techniques for investigating this.

No MeSH data available.


Related in: MedlinePlus

Single neuron activity related to second and subsequent syllables. Recordings from two electrodes at different depths in the same region of nondominant superior temporal gyrus during word listening. Neuron in channel 1 responds only to second and subsequent syllables of multisyllable words and not to single syllable words. Creutzfeldt and Ojemann, unpublished data [36].
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brainsci-03-00627-f003: Single neuron activity related to second and subsequent syllables. Recordings from two electrodes at different depths in the same region of nondominant superior temporal gyrus during word listening. Neuron in channel 1 responds only to second and subsequent syllables of multisyllable words and not to single syllable words. Creutzfeldt and Ojemann, unpublished data [36].

Mentions: The changes described above represent alterations in firing rates. However, a widely hypothesized model of the neuronal activity related to language involves temporal patterning. Some evidence for such temporal patterning related to language has been suggested based on recordings from subcortical nuclei [33] and a mechanism for temporal patterning of activity of individual neurons involving interactions with local field oscillations in the “gamma” range has been proposed [34]. In our lateral temporal recordings during language measures, we have identified only a few examples that seem to show some element of temporal patterning. During the auditory tasks, a neuron was identified during auditory listening that seemed to have the same patterns of activity during perception of particular phonemes ([14], Figure 2). Another neuron (in another patient) had similar selectivity to both auditory listening and overt repeating of the same word [15]. A few other neurons seemed to have patterns related to word structure, during auditory listening responding selectively to the second but not first syllable of multisyllable words (Figure 3) and also only compound words [14]. During the recent verbal memory paradigm described below, another neuron in another patient had significant overrepresentation of the interspike intervals in the 10–25 msec bins at encoding and retrieval, the two tasks requiring perception or production of the same name, compared to the different names used as distractors during memory storage [35]. These are hints, then that there may be temporal patterns for different words, perhaps reflecting different features of the word: phonemic structure, prosody, perhaps semantics, but if present, temporal patterns seem to be very sparsely coded. This question, of the role of temporal patterning compared to firing rate changes remains an important area for future investigation.


Human Temporal Cortical Single Neuron Activity during Language: A Review.

Ojemann GA - Brain Sci (2013)

Single neuron activity related to second and subsequent syllables. Recordings from two electrodes at different depths in the same region of nondominant superior temporal gyrus during word listening. Neuron in channel 1 responds only to second and subsequent syllables of multisyllable words and not to single syllable words. Creutzfeldt and Ojemann, unpublished data [36].
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4061841&req=5

brainsci-03-00627-f003: Single neuron activity related to second and subsequent syllables. Recordings from two electrodes at different depths in the same region of nondominant superior temporal gyrus during word listening. Neuron in channel 1 responds only to second and subsequent syllables of multisyllable words and not to single syllable words. Creutzfeldt and Ojemann, unpublished data [36].
Mentions: The changes described above represent alterations in firing rates. However, a widely hypothesized model of the neuronal activity related to language involves temporal patterning. Some evidence for such temporal patterning related to language has been suggested based on recordings from subcortical nuclei [33] and a mechanism for temporal patterning of activity of individual neurons involving interactions with local field oscillations in the “gamma” range has been proposed [34]. In our lateral temporal recordings during language measures, we have identified only a few examples that seem to show some element of temporal patterning. During the auditory tasks, a neuron was identified during auditory listening that seemed to have the same patterns of activity during perception of particular phonemes ([14], Figure 2). Another neuron (in another patient) had similar selectivity to both auditory listening and overt repeating of the same word [15]. A few other neurons seemed to have patterns related to word structure, during auditory listening responding selectively to the second but not first syllable of multisyllable words (Figure 3) and also only compound words [14]. During the recent verbal memory paradigm described below, another neuron in another patient had significant overrepresentation of the interspike intervals in the 10–25 msec bins at encoding and retrieval, the two tasks requiring perception or production of the same name, compared to the different names used as distractors during memory storage [35]. These are hints, then that there may be temporal patterns for different words, perhaps reflecting different features of the word: phonemic structure, prosody, perhaps semantics, but if present, temporal patterns seem to be very sparsely coded. This question, of the role of temporal patterning compared to firing rate changes remains an important area for future investigation.

Bottom Line: The majority of the changes in activity were tonic sustained shifts in firing.Patterned phasic activity for specific language items was very infrequently recorded.Human single neuron recordings provide a unique perspective on the biologic substrate for language, for these findings are in contrast to many of the findings from other techniques for investigating this.

View Article: PubMed Central - PubMed

Affiliation: Department of Neurological Surgery, University of Washington, Box 356470, Seattle, WA 98195, USA. gojemann@u.washington.edu.

ABSTRACT
Findings from recordings of human temporal cortical single neuron activity during several measures of language, including object naming and word reading are reviewed and related to changes in activity in the same neurons during recent verbal memory and verbal associative learning measures, in studies conducted during awake neurosurgery for the treatment of epilepsy. The proportion of neurons changing activity with language tasks was similar in either hemisphere. Dominant hemisphere activity was characterized by relative inhibition, some of which occurred during overt speech, possibly to block perception of one's own voice. However, the majority seems to represent a dynamic network becoming active with verbal memory encoding and especially verbal learning, but inhibited during performance of overlearned language tasks. Individual neurons are involved in different networks for different aspects of language, including naming or reading and naming in different languages. The majority of the changes in activity were tonic sustained shifts in firing. Patterned phasic activity for specific language items was very infrequently recorded. Human single neuron recordings provide a unique perspective on the biologic substrate for language, for these findings are in contrast to many of the findings from other techniques for investigating this.

No MeSH data available.


Related in: MedlinePlus