Luis C. Populin

Behavioral Studies of Sound Localization in the Cat

Using the magnetic search coil technique to measure eye and ear movements, we trained cats by operant conditioning to look in the direction of light and sound sources with their heads fixed. Cats were able to localize noise bursts, single clicks, or click trains presented from sources located on the horizontal and vertical meridians within their oculomotor range. Saccades to auditory targets were less accurate and more variable than saccades to visual targets at the same spatial positions. Localization accuracy of single clicks was diminished compared with the long-duration stimuli presented from the same sources. Control experiments with novel auditory targets, never associated with visual targets, demonstrated that the cats localized the sound sources using acoustic cues and not from memory. The role of spectral features imposed by the pinna for vertical sound localization was shown by the breakdown in localization of narrow-band (one-sixth of an octave) noise bursts presented from sources along the midsagittal plane. In addition, we show that cats experience summing localization, an illusion associated with the precedence effect. Pairs of clicks presented from speakers at (±18°,0°) with interclick delays of ±300 μsec were perceived by the cat as originating from phantom sources extending from the midline to approximately ±10°.

Fundamental differences between the thalamocortical recipient layers of the cat auditory and visual cortices

In visual and somatosensory cortices of several species, spiny stellate cells in layer 4 are the first elements in signal processing where thalamic information is integrated and emergent receptive field properties are generated and sent on to more superficial cortical layers. In vivo and in vitro experiments have provided important information about how the anatomy and physiology of these cells and this layer fit into the functional cortical circuitry. No such data exist for the auditory cortex but are requisite if we are to understand whether ideas about information processing in one sensory cortical area can be generalized to another. Accordingly, we used in vitro slices from which to record and labeled cells in the middle layers of the cat auditory and visual cortices to compare basic anatomical and physiological features of cells recovered in similar layers using the same methods. Our results demonstrate a striking difference in a basic characteristic of two primary sensory cortical areas. In the visual cortex, spiny stellate cells predominate, receive short‐latency synaptic inputs, and project to supergranular layers. No such spiny stellate population is encountered in the middle layers of the auditory cortex. Spiny cells that are not stellate or pyramidal are occasionally encountered but, as a group, do not display consistent anatomical or physiological features that might allow them to function as auditory cortical versions of the visual spiny stellates. Rather, pyramidal cells in the lower half of layer 3 and layer 4 appear to have assumed this role. J. Comp. Neurol. 436:508–519, 2001.

Monkey Sound Localization: Head-Restrained versus Head-Unrestrained Orienting

The sound localization abilities of three rhesus monkeys were tested under head-restrained and head-unrestrained conditions. Operant conditioning and the magnetic search coil technique were used to measure eye and head movements to sound sources. Whereas the results support previous findings that monkeys localize sounds very poorly with their heads restrained, the data also reveal for the first time that monkeys localize sounds much more accurately and with less variability when their heads are allowed to move. Control experiments using acoustic stimuli known to produce spatial auditory illusions such as summing localization confirmed that the monkeys based their orienting on localizing the sound sources and not on remembering spatial locations that resulted in rewards. Overall, the importance of using ecologically valid behaviors for studies of sensory processes is confirmed, and the potential of the rhesus monkey, the model closest to human, for studies of spatial auditory function, is established.

Anesthetics Change the Excitation/Inhibition Balance That Governs Sensory Processing in the Cat Superior Colliculus

The superior colliculus (SC) is a midbrain structure that plays a central role in the integration of information from different sensory modalities and the generation of orienting responses. Its normal function is thought to be governed by a strictly held balance between excitation and inhibition. This hypothesis was tested by recording from the same single units in the SC of cats before the injection of anesthetics, while anesthetics took effect, and after the injections during recovery. Sodium pentobarbital and ketamine, two agents commonly used in sensory physiology, were used. The results show a plethora of dose-dependent and nonlinear effects: the magnitude of evoked responses, receptive field properties, first spike latency, and bimodal integration were affected by both anesthetics in all units tested. Notably, prominent facilitation was observed at low levels of anesthesia, and inhibitory responses were changed into excitatory. Overall, the results challenge a fundamental tenet of sensory physiology: anesthesia, while decreasing single-unit responsiveness, leaves unaltered basic physiological properties.

Rhesus Monkeys (Macaca mulatta) Do Recognize Themselves in the Mirror: Implications for the Evolution of Self-Recognition

Self-recognition in front of a mirror is used as an indicator of self-awareness. Along with humans, some chimpanzees and orangutans have been shown to be self-aware using the mark test. Monkeys are conspicuously absent from this list because they fail the mark test and show persistent signs of social responses to mirrors despite prolonged exposure, which has been interpreted as evidence of a cognitive divide between hominoids and other species. In stark contrast with those reports, the rhesus monkeys in this study, who had been prepared for electrophysiological recordings with a head implant, showed consistent self-directed behaviors in front of the mirror and showed social responses that subsided quickly during the first experimental session. The self-directed behaviors, which were performed in front of the mirror and did not take place in its absence, included extensive observation of the implant and genital areas that cannot be observed directly without a mirror. We hypothesize that the head implant, a most salient mark, prompted the monkeys to overcome gaze aversion inhibition or lack of interest in order to look and examine themselves in front of the mirror. The results of this study demonstrate that rhesus monkeys do recognize themselves in the mirror and, therefore, have some form of self-awareness. Accordingly, instead of a cognitive divide, they support the notion of an evolutionary continuity of mental functions.

Postural muscle onset and voluntary movement in the elderly

In young and elderly subjects, push and pull arm movements were executed during sitting or standing, under both simple reaction (SR) and choice reaction (CR) conditions. The combined reaction time (RT) results showed that CRT was larger than SRT in both groups. While sitting, the young group exhibited only slight change in RT, whereas the elderly group showed sizeable RT decrease. During standing, for the SR condition, the elderlys RTs were slightly slower than the youngs; in contrast, for the CR condition, the elderlys RTs were substantially slower. Further, when the activation of ankle-stabilizer muscles was examined, it was found that postural muscle onset was essentially the same under both conditions. Focal-muscle onset and reaction time, under the choice condition, however, was sensitive to age-related differences. When these data are taken together, they suggest that the elderly may have an impaired postural system which is slow to stabilize the body prior to movement initiation.

Human sound localization: measurements in untrained, head-unrestrained subjects using gaze as a pointer

Studies of sound localization in humans have used various behavioral measures to quantify the observers’ perceptions; a non-comprehensive list includes verbal reports, head pointing, gun pointing, stylus pointing, and laser aiming. Comparison of localization performance reveals that in humans, just as in animals, different results are obtained with different experimental tasks. Accordingly, to circumvent problems associated with task selection and training, this study used gaze, an ethologically valid behavior for spatial pointing in species with a specialized area of the fovea, to measure sound localization perception of human subjects. Orienting using gaze as a pointer does not require training, preserves the natural link between perception and action, and allows for direct behavioral comparisons across species. The results revealed, unexpectedly, a large degree of variability across subjects in both accuracy and precision. The magnitude of the average angular localization errors for the most eccentric horizontal targets, however, were very similar to those documented in studies that used head pointing, whereas the magnitude of the localization errors for the frontal targets were considerably larger. In addition, an overall improvement in sound localization in the context of the memory-saccade task, as well as a lack of effect of initial eye and head position on perceived sound location were documented.

Dissociative effects of methylphenidate in nonhuman primates: Trade-offs between cognitive and behavioral performance

Low doses of methylphenidate reduce hyperactivity and improve attention in individuals with attention deficit hyperactivity disorder (ADHD) as well as in healthy humans and animals. Despite its extensive use, relatively little is known about its mechanisms of action. This study investigated the effects of methylphenidate on working memory performance, impulsivity, response accuracy and precision, and the ability to stay on task in rhesus monkeys using an oculomotor delayed response task. Methylphenidate affected task performance in an inverted-U manner in all three subjects tested. The improvements resulted from a reduction in premature responses and, importantly, not from improvement in the memory of target location. The length of time subjects participated in each session was also affected dose dependently. However, the dose at which the length of participation was maximally increased significantly impaired performance on the working memory task. This dissociation of effects has implications for the treatment of ADHD, for the nonprescription use of methylphenidate for cognitive enhancement, and for furthering the basic understanding of the neural substrate underlying these processes.

Decision making: effects of methylphenidate on temporal discounting in nonhuman primates.

Decisions are often made based on which option will result in the largest reward. When given a choice between a smaller but immediate reward and a larger delayed reward, however, humans and animals often choose the smaller, an effect known as temporal discounting. Dopamine (DA) neurotransmission is central to reward processing and encodes delayed reward value. Impulsivity, the tendency to act without forethought, is associated with excessive discounting of rewards, which has been documented in patients with attention deficit hyperactivity disorder (ADHD). Both impulsivity and temporal discounting are linked to the dopaminergic system. Methylphenidate (MPH), which blocks the DA transporter and increases extracellular levels of DA in the basal ganglia and prefrontal cortex, is a primary treatment for ADHD and, at low doses, ameliorates impulsivity in both humans and animals. This study tested the hypothesis that low doses of MPH would decrease the discounting rate of rhesus monkeys performing an intertemporal choice task, suggesting a reduction in impulsivity. The results support this hypothesis and provide further evidence for the role of DA in temporal discounting and impulsive behavior.

Target modality determines eye-head coordination in nonhuman primates: implications for gaze control

We have studied eye-head coordination in nonhuman primates with acoustic targets after finding that they are unable to make accurate saccadic eye movements to targets of this type with the head restrained. Three male macaque monkeys with experience in localizing sounds for rewards by pointing their gaze to the perceived location of sources served as subjects. Visual targets were used as controls. The experimental sessions were configured to minimize the chances that the subject would be able to predict the modality of the target as well as its location and time of presentation. The data show that eye and head movements are coordinated differently to generate gaze shifts to acoustic targets. Chiefly, the head invariably started to move before the eye and contributed more to the gaze shift. These differences were more striking for gaze shifts of <20-25° in amplitude, to which the head contributes very little or not at all when the target is visual. Thus acoustic and visual targets trigger gaze shifts with different eye-head coordination. This, coupled to the fact that anatomic evidence involves the superior colliculus as the link between auditory spatial processing and the motor system, suggests that separate signals are likely generated within this midbrain structure.