Auditory cortex lesions and auditory-visual associative learning in cats.
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The auditory cortex, located in the superior temporal gyrus, has been studied in squirrel monkeys with respect to its role in detecting species-specific vocalizations. Single neurons tested with selected vocalizations from the species' repertoire have been grouped into seven functional categories. Each category reflects a different level of processing with regard to vocalizations and artificial sounds. It is argued that, while the auditory cortex has the capability to detect and distinguish species-specific vocalizations, the interpretation of their biological significance likely takes place elsewhere.
Monkeys with lesions of auditory cortex were tested for their ability to localize the source of brief sounds. Although those deprived of primary auditory cortex bilaterally were able to indicate the direction of a sound with near-normal acuity, they were unable to locate its source. This dissociation of abilities suggest that the role of auditory cortex in sound localization is not so much sensory or perceptual as it is auditomotor or associative. Thus, sound localization joins loudness, pitch, and most other traditional attributes of sound as dimensions whose discrimination does not depend on auditory cortex. The question would now seem to turn to whether or not auditory cortex is necessary for any sensory discrimination whatever.
Afterdischarges in neurons of the auditory cortex (AI) were investigated in immobilized cats. The unit activity of 40% of neurons showed afterdischarges lasting 3--5 sec. after the cessation of the pure--tone or two--tone sound stimuli. Two--tone sound complexes consisted of the 1 st and higher harmonics with different phase relations between the components. The afterdischarges depended on some parameters of the sound stimuli. When tonal signal was used, 80% of neurons with obvious afterdischarges responded to the sound frequency. As regards the sensitivity to phase shifts in two--tone stimuli, changes of the activity occurred in 70% of cortical neurons with on-, off- and on--off reactions and were related to these components of the reaction. The pattern of afterdischarges in 19 of 32 neurons in the auditory cortex was also related to the phase shifts.
Research strategy in the auditory system has tended to parallel that in the visual system, where neurons have been shown to respond selectively to specific stimulus parameters. Auditory neurons have been shown to be sensitive to changes in acoustic parameters, but only rarely have neurons been reported that respond exclusively to only one biologically significant sound. Even at higher levels of the auditory system very few cells have been found that could be described as "vocalization detectors." In addition, variability in responses to artificial sounds have been reported for auditory cortical neurons similar to the response variability that has been reported in the visual system. Recent evidence indicates that the responses of auditory cortical neurons to species-specific vocalizations can also be labile, varying in both strength and selectivity. This is especially true of the secondary auditory cortex. This variability, coupled with the lack of extreme specificity in the secondary auditory cortex, suggests that secondary cortical neurons are not well suited for the role of "vocalization detectors."
Five normal rats and four rats with bilateral lesions of auditory cortex were tested by the conditioned suppression procedure to determine their abilities to discriminate between spatially separated sound sources. The discrimination involved detection of a change in location of a train of clicks from a speaker on the animals' left to a speaker on the right. The separation between speakers was varied from 180 degrees to 90 degrees, 45 degrees, 22 degrees, 12 degrees, 6 degrees, and psychophysical functions were obtained using a method of descending limits. Both normal and brain-damaged animals were capable of discriminating left from right clicks and psychophysical curves were similar for the two groups. Histological analysis indicated that the lesions in each of the four brain-damaged rats destroyed primary auditory cortex as well as surrounding belt areas. Therefore, for the rat, auditory cortex was not found to be essential for discrimination of the spatial locations of auditory stimuli. The results are discussed in light of impairments in sound localization following lesions of auditory cortex in other mammalian species.
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Auditory-evoked responses in single neurons from rhesus monkey auditory cortex were measured under four relatively well defined behavioral and physiological conditions: (1) monkey awake and performing a simple auditory reaction time task; (2) monkey awake but not performing a task (Stage A); (3) monkey in a drowsy or Stage 1 sleep state (State B); and (4) monkey anesthetized with a short-acting nonbarbiturate anesthetic. For most units studied the response evoked by the auditory stimulus was greater in the performance condition than in the nonperformance condition. Similarly, evoked activity was usually greater in State A than in State B. Finally, evoked responses under anesthesia were usually weaker than those obtained in the unanesthetized animal. Some exceptions were noted in each case. Differences in response patterns and in rate versus intensity functions of neurons were also found to be associated with the behavioral and physiological state of the preparation. No significant changes in unit spontaneous activity associated with changes in behavioral or physiological condition were observed.
1. Cats with one cochlea destroyed were trained to localize sound. After behavioral measures of the animal's accuracy of localization were made, cortical auditory areas were ablated unilaterally. 2. The results showed: a) like binaural localization, monaural localization of sound in space, as measured by the ability of an animal to move toward a sound source, depends on integrity of auditory cortex; b) it is only ablation of cortex contralateral to the functional ear that seriously affects localizing behavior; ablation of cortex ipsilateral to the intact cochlea has little or no effect on localizing behavior. 3. To explain the results, we suggest that auditory cortex is essential for an organized perception of space including the relation of the animal's position to other objects in space. We also suggest that auditory cortex contralateral to a given ear is necessary in order for the animal to recognize that a stimulus is presented to that ear of, when both ears are intact, to recognize that the stimulus to the given ear differs in some way (intensity, time of arrival, sequential arrangement of sounds) from the stimulus to the opposite ear.
The prospective auditory cortex was analysed in human fetuses at 11--13,5 post-ovulatory weeks with Nissl, Golgi and E.M. techniques. At 11--12 weeks, marginal, cortical plate, intermediate, subventricular and ventricular layers were recognized. Post-migratory neurons with developing dendrites were seen in marginal layer, cortical plate and superficial part of the intermediate zone only. At 12--13,5 weeks the superficial part of the intermediate zone is transformed into the true cortical layer--"subplate layer"--characterized by maturing neurons with growing dendrites, fine axonal arborization and low cell density. The neuronal circuitry elements are thus present very early in the prospective auditory cortex and distributed throughout the deep cortical plate of the "subplate layer" corresponding to the synaptic territory of other areas of the human fetal cortex.
The character of interneuronal relations in the auditory cortex of alert and anaesthetized cats (nembutal) with chronicly inplanted electrodes was studied with the method of statistic analysis of cross-intervals of the two impulse series. The analysis of the histograms, obtained by means of processing a neuronal activity, showed that nembutal did not eliminate the dependent relations between neurones and that in the majority of cases the types of these relations are either retained or supplemented with new components. Experiments with a reduced dose of nembutal permitted to trace in time the changes in the amount of the inhibitory and excitatory interrelations in the anaesthetized state, and to compare these changes to the changes in the frequency of spike activity. It was found that nembutal predominantly suppresses the activity of the neurones, generating small spikes. The number of inhibitory connections is reduced simultaneously. Such synchroneity permits to assume the participation of the neurones generating small spikes in the establishment of inhibitory interrelations in the cat auditory cortex.
Development of the response of the auditory cortex to unilateral acoustic stimulation by a chick was studied in guinea-pig foetuses from the 50th day to the end of gestation and in newborn animals. The first cortical response appeared on the 52nd to 53rd day of gestation. The maximum responses were concentrated in the temporal cortex, between the somatosensory (parietal) and optic (occipital) area. The progressive development of the latent period of the cortical response and of its various components distinctly slowed down on the last days of gestation. At the same time, the amplitude of the cortical response was temporarily augmented. The cortical response developed from a simple negative wave in the youngest embryos into an intricate complex with an initial positive component in newborn guinea-pigs. The basic components of this complex were already discernible on the 64th to 65th day of gestation. The ability to react to repeated peripheral stimulation of 0.1-2 c/s frequency increased with foetal age, with temporary deterioration on the last days of gestation. Resistance of the cortical auditory response to cerebral anoxia rose up to term, with a temporary drop from the 64th day of gestation. After the initiation of independent respiration, cerebral hypoxia and bilateral vagotomy chiefly influenced the stability of the more recent components of the cortical auditory response in mature foetuses.
The basal dendritic trees of layer V pyramidal cells in the rat auditory cortex were examined quantitatively in a group of 3-month-old and a group of 34- and 36-month-old rats. Two forms of analysis were used on the Golgi preparations: (1) the number of intersections between the basal dendrites and a series of concentric circles whose common center lies over the perikaryon center, and (2) the number of dendritic branches, by order, per neuron. The data indicate that in the old animals the density of the dendritic tree has decreased significantly within a radius of about 150mu of the perikaryon, yet the extent of the dendritic domain has not changed appreciably. Analysis of the dendritic branching suggests that there has been a deterioration not only in the peripheral branches of the dendritic tree, but also that entire dendrites have been lost. This loss of primary branches was confirmed through the reconstruction of layer V neuronal perikarya and their proximal dendrites from 1-mu plastic serial sections of auditory cortex. Concomitant with the loss of dendrites which accompanies advancing age is a tendency for the perikaryon to be smaller, but not distorted, in the old animals.
The study investigated, in primary auditory cortex (AI) of awake cats, the relationship over a range of stimuli between the amplitude and latency of the initial positive deflection (P1) of the primary evoked potential and the intensity of concurrent underlying evoked single unit activity. Epidural evoked potentials and extracellular responses of 155 single units to monaural 100 musec clicks ranging from 45 to 110 dB were recorded. At low stimulus levels, considerable unit response could occur with a very small P1. At middle stimulus levels, unit response was directly proportional to P1 amplitude. At higher stimulus levels, P1 amplitude continued to increase while unit response began to saturate.
1. Dogs with bilateral auditory cortex lesions were tested on their ability to localize and discriminate brief sounds. In each test the animals were required to approach one of two goal boxes in order to indicate their response. 2. The results showed: a) that the operated animals could not solve the localization tasks when the goal boxes were located more than 125 cm away, but could solve the task if the goal boxes were located closer to the animal; b) that the operated animals could successfully discriminate brief bursts of click trains (i.e., 100/s versus 10/s, 0.3 s duration) even when required to indicate their discrimination by moving to goal boxes located 250 cm away, in spite of the fact that they could not successfully localize these sounds under similar conditions; c) that the operated animals tracked the source of a continuous sound instead of localizing it in a normal manner. 3. It appears that the deficit in sound localization resulting from cortical ablation is not due to any impairment in auditory attention or memory. Furthermore, the deficit cannot be ascribed to an inability to make a spatial response to an auditory cue. Instead, the deficit may be the result of a disconnection of the sound-localization mechanism from the motor mechanism necessary for some, though not all, behavioral responses.
Single-unit responses were recorded from the auditory cortex of rhesus monkeys that were performing an auditory selective attention task. Acoustic stimuli were presented randomly to either the left or right ear through headphones. In a given block of trials one ear was selected as the ear to be attended, and was indicated by lighting either a left or right response key. The animal's task was to press the lighted key whenever stimuli were presented to the attended ear, but to make no response to stimuli presented to the other ear. The attended ear was alternated on successive blocks of trials. Fourteen of 77 units showed significantly greater rates of evoked discharges for an attended stimulus than for an identical non-attended stimulus. The increase in stimulus-evoked activity was not accompanied by any increase in spontaneous activity or by any changes in the pattern of a unit's response. Changes in firing rate occurred at latencies as early as 20 msec.
Single-unit responses were recorded from the auditory cortex of rhesus monkeys performing a selective atteintion task which used combined light and sound stimuli. The animals were first trained to push a lever to the left for a noise burst and to the right for a tone burst, and then trained to push left for a left light and right for a right light. Subsequently, one of the four possible light and sound stimulus combinations (Noise + Left Light, Noise + Right Light, Tone + Left Light, Tone + Right Light) was randomly presented on each trial. In blocks of 100 trials only one part of the combined stimulus (either the light or the sound) determined the direction of lever push that would be reinforced. Responses of single units to identical sound stimuli were compared for blocks in which sound was the relevant cue and blocks in which light was the relevant cue. Typically, differences were in response strength without alteration of response pattern. Even the earliest response components (15-20 msec latency) could show changes. Two-thirds of the response comparisons showed differences in strength depending upon whether sound or light was the relevant cue, with about as many responses stronger for light relevant as for sound relevant. Independent of which modality was relevant, unit responses for trials in which both parts of the combined light and sound stimulus indicated the same direction of lever push were generally stronger than unit responses for trials in which the two parts of the combined stimulus signalled opposite directions of lever pushes.
The activity of 28 cells located mainly in the secondary auditory cortex (A II) of awake squirrel-monkeys, was extracellularly recorded for periods of up to 6 h. Seven different species-specific vocalizations, which were repeatedly presented to the monkey, were used as auditory stimuli. Twenty-six cells responded, at least once, to one or more vocalizations; 22 cells revealed some change in their response (pattern or strength) to at least one vocalization ("change in response"). Twenty-one cells exhibited a change in the number and/or type of vocalization to which they responded during the recording period ("change in selectivity"). At some time during the recording period all the responding cells exhibited a "change in response" and/or a "change in selectivity" ("change in responsiveness"). A "change in response" of a cell to a vocalization did not necessarily exclude a "change in selectivity", associated with the same vocalization, later in time and vice-versa. A "change in responsiveness" to one vocalization was not necessarily correlated with "changes in responsiveness" to other vocalizations.