Consonance and dissonance of musical chords: neural correlates in auditory cortex of monkeys and humans.

Some musical chords sound pleasant, or consonant, while others sound unpleasant, or dissonant. Helmholtz's psychoacoustic theory of consonance and dissonance attributes the perception of dissonance to the sensation of "beats" and "roughness" caused by interactions in the auditory periphery between adjacent partials of complex tones comprising a musical chord. Conversely, consonance is characterized by the relative absence of beats and roughness. Physiological studies in monkeys suggest that roughness may be represented in primary auditory cortex (A1) by oscillatory neuronal ensemble responses phase-locked to the amplitude-modulated temporal envelope of complex sounds. However, it remains unknown whether phase-locked responses also underlie the representation of dissonance in auditory cortex. In the present study, responses evoked by musical chords with varying degrees of consonance and dissonance were recorded in A1 of awake macaques and evaluated using auditory-evoked potential (AEP), multiunit activity (MUA), and current-source density (CSD) techniques. In parallel studies, intracranial AEPs evoked by the same musical chords were recorded directly from the auditory cortex of two human subjects undergoing surgical evaluation for medically intractable epilepsy. Chords were composed of two simultaneous harmonic complex tones. The magnitude of oscillatory phase-locked activity in A1 of the monkey correlates with the perceived dissonance of the musical chords. Responses evoked by dissonant chords, such as minor and major seconds, display oscillations phase-locked to the predicted difference frequencies, whereas responses evoked by consonant chords, such as octaves and perfect fifths, display little or no phase-locked activity. AEPs recorded in Heschl's gyrus display strikingly similar oscillatory patterns to those observed in monkey A1, with dissonant chords eliciting greater phase-locked activity than consonant chords. In contrast to recordings in Heschl's gyrus, AEPs recorded in the planum temporale do not display significant phase-locked activity, suggesting functional differentiation of auditory cortical regions in humans. These findings support the relevance of synchronous phase-locked neural ensemble activity in A1 for the physiological representation of sensory dissonance in humans and highlight the merits of complementary monkey/human studies in the investigation of neural substrates underlying auditory perception.

Auditory cortex on the human posterior superior temporal gyrus.

The human superior temporal cortex plays a critical role in hearing, speech, and language, yet its functional organization is poorly understood. Evoked potentials (EPs) to auditory click-train stimulation presented binaurally were recorded chronically from penetrating electrodes implanted in Heschl's gyrus (HG), from pial-surface electrodes placed on the lateral superior temporal gyrus (STG), or from both simultaneously, in awake humans undergoing surgery for medically intractable epilepsy. The distribution of averaged EPs was restricted to a relatively small area on the lateral surface of the posterior STG. In several cases, there were multiple foci of high amplitude EPs lying along this acoustically active portion of STG. EPs recorded simultaneously from HG and STG differed in their sensitivities to general anesthesia and to changes in rate of stimulus presentation. Results indicate that the acoustically active region on the STG is a separate auditory area, functionally distinct from the HG auditory field(s). We refer to this acoustically sensitive area of the STG as the posterior lateral superior temporal area (PLST). Electrical stimulation of HG resulted in short-latency EPs in an area that overlaps PLST, indicating that PLST receives a corticocortical input, either directly or indirectly, from HG. These physiological findings are in accord with anatomic evidence in humans and in nonhuman primates that the superior temporal cortex contains multiple interconnected auditory areas.

Temporal encoding of the voice onset time phonetic parameter by field potentials recorded directly from human auditory cortex.

Voice onset time (VOT) is an important parameter of speech that denotes the time interval between consonant onset and the onset of low-frequency periodicity generated by rhythmic vocal cord vibration. Voiced stop consonants (/b/, /g/, and /d/) in syllable initial position are characterized by short VOTs, whereas unvoiced stop consonants (/p/, /k/, and t/) contain prolonged VOTs. As the VOT is increased in incremental steps, perception rapidly changes from a voiced stop consonant to an unvoiced consonant at an interval of 20-40 ms. This abrupt change in consonant identification is an example of categorical speech perception and is a central feature of phonetic discrimination. This study tested the hypothesis that VOT is represented within auditory cortex by transient responses time-locked to consonant and voicing onset. Auditory evoked potentials (AEPs) elicited by stop consonant-vowel (CV) syllables were recorded directly from Heschl's gyrus, the planum temporale, and the superior temporal gyrus in three patients undergoing evaluation for surgical remediation of medically intractable epilepsy. Voiced CV syllables elicited a triphasic sequence of field potentials within Heschl's gyrus. AEPs evoked by unvoiced CV syllables contained additional response components time-locked to voicing onset. Syllables with a VOT of 40, 60, or 80 ms evoked components time-locked to consonant release and voicing onset. In contrast, the syllable with a VOT of 20 ms evoked a markedly diminished response to voicing onset and elicited an AEP very similar in morphology to that evoked by the syllable with a 0-ms VOT. Similar response features were observed in the AEPs evoked by click trains. In this case, there was a marked decrease in amplitude of the transient response to the second click in trains with interpulse intervals of 20-25 ms. Speech-evoked AEPs recorded from the posterior superior temporal gyrus lateral to Heschl's gyrus displayed comparable response features, whereas field potentials recorded from three locations in the planum temporale did not contain components time-locked to voicing onset. This study demonstrates that VOT at least partially is represented in primary and specific secondary auditory cortical fields by synchronized activity time-locked to consonant release and voicing onset. Furthermore, AEPs exhibit features that may facilitate categorical perception of stop consonants, and these response patterns appear to be based on temporal processing limitations within auditory cortex. Demonstrations of similar speech-evoked response patterns in animals support a role for these experimental models in clarifying selected features of speech encoding.

Cochleo- and tonotopic organization of the second auditory cortical area in the cat.

The cochleo- and tonotopic organization of the second auditory area (AII) was investigated in cats anaesthetized with pentobarbital using a combination of macro- and microelectrode recording technique. The results obtained following electrical stimulation of the neural fibres innervating different regions of the organ of Corti indicate the existence of two complete representations of the cochlea in area AII: one in the dorsocaudal portion, the other in its ventrorostral portion. These two cortical representations of the cochlea differ in size and spatial orientation. The dorsocaudal projection area extends over a distance of 2.6-3.2 mm from the basal to the apical focus and is arc-shaped. The spatial orientation of cochlea representation within the dorsocaudal region of AII is similar to that described in AI, in that stimulation of the cochlea base results in maximal responses in the more rostral portion of AII and stimulation of the apex evokes cortical responses more caudally. The ventrorostral region within AII is smaller (1.4-2.5 mm length), and has the opposite cochleotopic orientation (base and apex stimulation represented caudally and rostrally, respectively). In both AII zones, there was a proportionally greater cortical representation of basilar membrane than of middle and apical portions. Although two distinct zones with the overall cochleotopic pattern described above were noted in all cats, their precise size and location considerably varied in different animals. Using microelectrode recordings, a cortical tonotopic organization can be observed that was consistent with and expanded on the earlier cochleotopic data. Within the dorsocaudal region of AII, neurons with higher best frequency responses were located in more rostral regions, while those with lower best frequencies were located caudally. An orderly progression of best frequency responses was noted as serial recordings carried out along the full extent of the representation. Neurons within the ventrorostral region of AII also displayed an orderly progression of best frequencies, but in the opposite direction, with higher best frequencies noted more caudally and lower best frequencies more rostrally.

An integrated multipurpose lesion-making electrode.

PURPOSE: Although excellent results are reported from centers using microelectrode mapping during stereotactic pallidotomy, the recording methods used are time-consuming and technically cumbersome. We sought to develop a new electrode concept that may, when eventually applied in clinical practice, improve the efficiency and safety of microelectrode-guided functional neurosurgical procedures. CONCEPT: The scout electrode uses a recently developed research technique for simultaneously obtaining multiple microelectrode recordings along the shaft of a macroelectrode. RATIONALE: By positioning recording sites on either side of a lesion-making contact, it is possible to functionally "scout" the brain tissue surrounding the proposed lesion site, thus eliminating the need for serial movements and electrode interchanges. DISCUSSION: The feasibility of the scout electrode concept was tested using prototypes placed into cat medial geniculate nucleus. High-quality unit recordings were simultaneously obtained from different regions within the medial geniculate nucleus. This ability to physiologically map sites above and below the lesion-making contact facilitated precise placement of radiofrequency lesions in the center of the medial geniculate nucleus. These results suggest that it may be possible to develop clinically useful devices based on this novel concept.

Chronic microelectrode investigations of normal human brain physiology using a hybrid depth electrode.

Neurosurgeons have unique access to in vivo human brain tissue, and in the course of clinical treatment important scientific advances have been made that further our understanding of normal brain physiology. In the modern era, microelectrode recordings have been used to systematically investigate the cellular properties of lateral temporal cerebral cortex. The current report describes a hybrid depth electrode (HDE) recording technique that was developed to enable neurosurgeons to simultaneously investigate normal cellular physiology during chronic intracranial EEG recordings. The HDE combines microelectrode and EEG recordings sites on a single shaft. Multiple microelectrode recordings are obtained from MRI defined brain sites and single-unit activity is discriminated from these data. To date, over 60 HDEs have been placed in 20 epilepsy surgery patients. Unique physiologic data have been gathered from neurons in numerous brain regions, including amygdala, hippocampus, frontal lobe, insula and Heschl's gyrus. Functional activation studies were carried out without risking patient safety or comfort.

A chronic microelectrode investigation of the tonotopic organization of human auditory cortex.

We investigated the functional organization of human auditory cortex using a new chronic microelectrode technique. Tonotopic mapping data was obtained at the single unit level for the first time in humans. All sound-driven units were noted to have frequency-dependent response patterns. The majority of units (73%) demonstrated sharply tuned excitatory best-frequency responses. Twenty seven percent of units showed wide receptive fields, representing excitatory responses to almost the entire range of frequencies presented. A tonotopic pattern was observed with best frequencies systematically increasing as more medial-caudal recording sites were sampled.

A hybrid clinical-research depth electrode for acute and chronic in vivo microelectrode recording of human brain neurons. Technical note.

For several decades, important scientific information has been gained from in vivo microelectrode recordings of individual human cerebral cortical neurons in patients with epilepsy. The experimental methods used, however, are technically complex and require a highly skilled intraoperative team. There are also significant experimental time limitations, as well as constraints on the type of behavioral tests conducted, and the brain regions that may be safely studied. In this report, a new method is described for obtaining in vivo microelectrode recordings using a hybrid depth electrode (HDE). High-impedance research recording contacts are interspersed between low-impedance clinical electroencephalographic (EEG) contacts along the HDE shaft. The HDE has the same external physical properties as a standard clinical depth electrode (DE). Following preclinical laboratory testing, 15 HDEs were used in the evaluation of six patients with medically refractory epilepsy. High-quality EEG recordings were obtained in all cases (two acute intraoperative, four from the chronic epilepsy monitoring unit). Action potentials from individual neurons were successfully recorded during all experimental sessions; however, the chronic preparations were clearly superior. Chronic HDEs are placed using a standard stereotactic system, and the locations of recording contacts are documented on a postimplantation imaging study. The quality of the chronic research recordings was excellent over study periods ranging from 5 to 14 days. The patients rested comfortably on the ward and were able to cooperate with complex experimental instructions. Basic neuroscientists participated fully in all aspects of the chronic investigations. The use of an HDE in place of a standard clinical DE may now allow detailed physiological investigations of any brain region targeted for clinical DE implantation.

Peculiarities of inhibition in cat auditory cortex neurons evoked by tonal stimuli of various durations.

The extra- and intracellular responses of 262 neurons in A1 to tones of best frequency with durations ranging from 10 ms to 1.2 min were studied acute experiments on ketamine-anesthetized cats. Following the generation of action potentials in response to the tone stimulus, inhibition of both the background and the auditory stimulus-evoked spike activity were observed in 91% of the investigated neurons. The duration of this inhibition corresponded to the stimulus duration. For the remaining neurons (9%) an inhibition of the stimulus-evoked spike activity alone was seen, also corresponding to the stimulus duration. Maximal inhibition of the spike activity occurred for the first 100-200 ms of the inhibitory response (the period which equalled the time of development of an IPSP in a cell). During this period of IPSP development, the membrane resistance of the neuron was reduced to 60-90% of its initial value. Varying the duration of the acoustic signal within a range of 10-200 ms was accompanied by a change in the IPSP duration and inhibition of the spike activity of the neuron. Whenever the tone lasted more than 200 ms, the membrane potential of the neuron was restored to the resting potential. However, during this period, the responsiveness of the neuron was lower than that initially observed. Measurement of the membrane resistance during the inhibitory pause that was not accompanied by hyperpolarization produced an index with an average 17% lower than the initial value for 87% of the neurons.(ABSTRACT TRUNCATED AT 250 WORDS)

Formation of spike response to sound tones in cat auditory cortex neurons: interaction of excitatory and inhibitory effects.

Responses of the auditory cortical neurons to sound tones were studied extra- and intracellularly in anaesthetized cats. The pattern of response to tone stimuli could most differ in neurons tuned to the same sound frequency and forming a vertical cortical column. Phasic reactions were found in 69% of the neurons studied. Such neurons were encountered in all cortical layers but about 50% of them were localized at a depth of 0.4-1.0 mm, which corresponds to layers III and IV of the auditory cortex. Neurons with phasic reactions were able to respond to a relatively narrow frequency band that demonstrates high discriminative ability of these cells to the frequency analysis of sound signals. Inhibitory processes realized via both forward afferent and recurrent intracortical inhibition mechanisms play particular roles in the formation of phasic reaction of such neurons to different frequency tones. Twenty-six per cent of neurons generated tonic responses to the sound. The majority of such cells (94%) were localized at a depth of 1.0-2.2 mm, which corresponds to cortical layers V and VI. Inhibitory processes exert a much lesser influence on formation of tonic responses in comparison with phasic ones. Neurons of the tonic type, in contrast to phasic neurons, respond to a wider frequency band; their lower ability to discriminate sound frequency is obvious. Parameters of the responses of tonic neurons strictly correlated with the duration and intensity of the acoustic signal. The possibility of some tonic neurons playing an inhibitory role in auditory cortex is discussed [Volkov I. O. et al. (1989) Neurophysiology, Kiev 21, 498-506, 613-620 (in Russian)]. A small portion of the auditory area AI neurons (2%) demonstrated the suppression of background activity during tone stimulation. They were localized mainly in deep cortical layers (V and VI). Intracortical inhibition is supposed to play a dominant role in the formation of this type of response. About 3% of the studied auditory cortex neurons with background activity generated no response to tonic stimuli. Such cells were usually encountered in the superficial auditory cortex layers (I and II).

[Reactions of tonic-type neurons in the cat auditory cortex to tones of various frequency and intensity]. / Reaktsii neironov tonicheskogo tipa slukhovoi kory koshki na tony raznoi chastoty i intensivnosti.

Extra- and intracellularly recorded responses of the acoustic cortex neurons to sound tones of different frequency and intensity and peculiarities of the organization of receptive fields of these units were studied in immobilized cats. Special attention was paid to neurons with tonic spike responses to these stimuli. Such tonic-type neurons were met in different cortical layers but most of them (93%) were localized at depth of 1.0-2.2 mm. Mean response threshold of these cells was lower by 7.7 dB than that of phasic-type neurons. Tonic-type units were characterized by lower frequency-discriminative ability in comparison with phasic ones: mean values of Q10 were 4.1 +/- 0.4 and 9.1 +/- 0.7, respectively. Dimensions of receptive fields of tonic-type units were 3.5 times as large as those of phasic ones. Most of tonic-type neurons (80%) differed from phasic ones in 1.5-2.0 time shorter action potentials. Tonic neurons demonstrated high sensitivity to variations of duration and intensity of the acoustic stimulation.

[The interaction of neurons characterized by a tonic reaction to sound with other neurons in the cat auditory cortex]. / Vzaimodeistvie neironov, kharakterizuiushchikhsia tonicheskoi reaktsiei na zvuk, s drugimi neironami v slukhovoi kore koshki.

Interaction of neurons with tonic response to sound with adjacent or distant (approximately 400-500 micrograms) cortex neurons was studied in acute experiments on 15 immobilized cats using a method of the cross-correlation analysis. A presence of synchronizing excitatory input common for the cells has been revealed in 26 pairs (72%) on the cross-correlograms. The results of the cross-correlation analysis in five pairs of neurons show mono- or polysynaptic excitatory effect of a tonic neuron to impulse activity of another neuron. Negative correlation indicative of the inhibitory influence of tonic neurons on impulse responses of other neurons of the same or adjacent auditory cortex column is revealed in five pairs of neurons, but the inhibitory influences may be considered as monosynaptic ones only in 3 pairs of these neurons (latency of interaction 1.0-1.5 ms). The data obtained permit concluding that the group of neurons characterized by tonic response to sound is a heterogeneous one in the functional respect. An assumption that some neurons of the tonic type are inhibitory interneurons of the auditory cortex, other excitatory ones is under discussion.

[Tonotopic organization of the dorsocaudal zone of auditory area AII of the cerebral cortex in the cat]. / Chastotnotopicheskaia organizatsiia dorsokaudal'noi zony slukhovoi oblasti AII kory mozga koshi.

Tonotopic organization of dorsocaudal zone of secondary auditory area (AII) was studied in acute nembutal-anaesthetized cats. Neurons of this zone responded selectively to acoustic stimuli of definite frequencies. 74% of units had one best frequency. 26% of units had several best frequencies while 7% responded in all the range tested and had no best frequency. Neurons with low best frequencies were localized in upper part of sylvian gyrus near posterior ectosylvian sulcus. Successive increase of best frequencies occurred during ventrorostral shifting of the recorded point along the sylvian gyrus. The distance between low frequency and high frequency foci in the dorsocaudal projection zone was 2.5-3.5 mm. Neurons with close values of best frequency organized in vertical columns could differ substantially as to dimensions of receptive fields, precision of frequency selectivity and patterns of impulse responses.

[Effect of penicillin on the discrimination function of the auditory cortex neurons in the cat]. / Vliianie penitsillina na diskriminatsionnuiu funktsiiu neironov slukhovoi kory koshki.

Responses and receptive fields of neurons in auditory cortex (AI) were studied in acute nembutal-anaesthetized cats before and during ionophoretic application of penicillin. Frequency and duration of impulse responses to tone bursts were increased during application in the majority (83%) of neurons. Increase of receptive fields and decline of frequency selectivity were found in 80% of neurons. The data obtained are regarded as proofs of decisive role of GABA-ergic inhibition in formation of functional receptive fields of auditory cortical neurons.

[Characteristics of the responses of auditory cortex neurons in the cat to tonal stimulation during nembutal anesthesia and after recovery from it]. / Kharakteristika reaktsii neironov slukhovoi kory koshki na tonal'nuiu stimuliatsiiu vo vremia nembutalovogo narkoza i posle vykhoda iz nego.

Responses of auditory (AI) cortex neurons to tonal (1-25 kHz) stimulation were studied in cats under and after nembutal anaesthesia. Patterns of responses recorded during first hours and 10-30 hours after nembutal injection differed essentially. Most (89%) of neurons of anaesthetized cat had no background activity and produced stereotypical on-responses to tonal stimulation with the best frequency. Off-effects were usually absent. Variability of responses increased substantially after cessation of anesthesia. On-, on-off- and off-responses were obvious in 76% of neurons, approximately 21% of neurons tonically increased or decreased spike activity during the stimulus action. Duration of the stimulus action was reflected in response characteristics of the overwhelming majority of AI cortical neurons.

[Reactions of neurons of the auditory cortex of unanesthetized cats to tones of a characteristic frequency]. / Reaktsii neironov slukhovoi kory nenarkotizirovannykh koshek na tony kharakteristicheskoi chastoty.

Extra- and intracellular responses of primary auditory cortex (AI) neurons were studied in acute experiments on non-anaesthetized cats. It was found that auditory cortex neurons having similar best frequencies revealed various forms of responses to corresponding frequency tones. Neurons responded to the tone by on reactions constituted about 40% of nerve cells studied. 27% of neurons revealed responses of on-off and off types. 27% of cortical neurons responded by steady excitation or by inhibition of background activity. About 6% of neurons did not respond to the tone. During intracellular recordings about 85% of neurons studied responded to switching on and/or off of the tone by a spike-IPSP sequence. 96% of cortical neurons generated IPSP as a constant component of the response to tone. Tonic responses of auditory cortical neurons were the result of powerful and lasting depolarization of the postsynaptic membranes. The conclusion is made that interaction of excitatory and inhibitory processes is the most significant in any kind of responses of the auditory cortical neurons to tones.

[Characteristics of post-spike and lateral inhibition in neurons of the primary auditory cortex in the cat]. / Kharakteristika postimpul'snogo i lateral'nogo tormozheniia v neironakh pervoi slukhovoi oblasti kory mozga koshki.

In experiments on cats anaesthetized with nembutal it was shown by intracellular recordings that neurons located in the primary auditory cortex respond to characteristic frequency tones or to electrical stimulation of spiral ganglion fibres innervating the centre of the neuronal receptive field by a short latency spike response followed by long-lasting (20-250 ms) poststimulus inhibition. The cause of this inhibition is an IPSP originating in the studied neuron after the spike. On the basis of close connection between poststimulus inhibition and preceding spike activity the conclusion is made that the inhibition is created by a recurrent mechanism. When tones of noncharacteristic frequencies were used or peripheral parts of the receptive field were stimulated, responses in form of EPSP-IPSP developed. They were followed by depression of neuronal background activity and its responses to test stimuli. It was shown that these effects are produced by the mechanism of lateral inhibition. The characteristics of these two kinds of inhibition are presented.

[Intracellular reactions of neurons of the primary auditory area of the cerebral cortex in the cat to tones of different frequency and electric stimulation of nerve fibers of the spiral ganglion]. / Vnutrikletochnye reaktsii neironov pervoi slukhovoi oblasti kory mozga koshki na tony raznoi chastoty i élektricheskoe razdrazhenie nervnykh volokon spiral'nogo gangliia.

In experiments with nembutal-anaesthetized cats it was found that neurons in the AI auditory cortical area responded to sound stimulation by EPSP, EPSP-spike-IPSP, EPSP-IPSP and IPSP. The majority of neurons studied responded to tones of characteristic frequency or to above-threshold tones whose frequencies were close to the characteristic ones as well as to electrical stimulation of spiral ganglion fibres innervated a central part of the receptive field by the sequence: EPSP-spike-IPSP. Tones whose frequency differed significantly from the characteristic one and electrical stimulation of the peripheral parts of the receptive field evoked responses in the form of EPSP-IPSP or IPSP. The tone frequency band that under threshold stimulation evoked a spike in a neuron was significantly narrower than the tone frequency band that evoked EPSP or IPSP. Two types of IPSPs were observed: components of the EPSP-spike-IPSP sequence evoked by excitation of receptors in the centre of the receptive field and primary or following EPSP evoked only if receptors locating in peripheral parts of the receptive field were excited.