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The overlapping roles of the inner ear and lateral line: the active space of dipole source detection.

The problems associated with the detection of sounds and other mechanical disturbances in the aquatic environment differ greatly from those associated with airborne sounds. The differences are primarily due to the incompressibility of water and the corresponding increase in importance of the acoustic near field. The near field, or hydrodynamic field, is characterized by steep spatial gradients in pressure, and detection of the accelerations associated with these gradients is performed by both the inner ear and the lateral line systems of fishes. Acceleration-sensitive otolithic organs are present in all fishes and provide these animals with a form of inertial audition. The detection of pressure gradients, by both the lateral line and inner ear, is the taxonomically most widespread mechanism of sound-source detection amongst vertebrates, and is thus the most likely primitive mode of detecting sound sources. Surprisingly, little is known about the capabilities of either the lateral line or the otolithic endorgan in the detection of vibratory dipole sources. Theoretical considerations for the overlapping roles of the inner ear and lateral line systems in midwater predict that the lateral line will operate over a shorter distance range than the inner ear, although with a much greater spatial resolution. Our empirical results of dipole detection by mottled sculpin, a benthic fish, do not agree with theoretical predictions based on midwater fishes, in that the distance ranges of the two systems appear to be approximately equal. This is almost certainly as a result of physical coupling between the fishes and the substrate. Thus, rather than having a greater active range, the inner ear appears to have a reduced distance range in benthic fishes, and the lateral line distance range may be concomitantly extended.

Animals↗

Central and parietal event-related lateralizations in a flanker task.

Recently Wascher et al. (1999) reported that in a flanker task with arrow stimuli not only the known lateralized readiness potential (LRP) that reflects lateralized response activation was induced, but also a parietal lateralized activation (direction encoding lateralization; DEL) that was interpreted as reflecting an earlier coding of a response side. However, the Wascher study did not exclude that the DEL could have also been due to lateralized stimulus- or attention-related factors. In the present study we used vertically directed arrow stimuli, and had our subjects perform responses in the vertical dimension. To separate flanker-induced from target-induced lateralizations the delay between the presentations of irrelevant and relevant stimuli (stimulus onset asynchrony; SOA) was manipulated. Apart from the usual LRPs we obtained clear DELs that varied in a similar way with the experimental variables, but peaked earlier and had a more posterior topography than the LRP. These results indicate that the DEL reflects premotor response representation.

Adult↗

Semiology of temporal lobe seizures: value in lateralizing the seizure focus.

PURPOSE: To determine the lateralizing value of the clinical manifestations of seizures in patients with temporal lobe epilepsy (TLE), we made a retrospective videotape analysis of complex partial seizures (CPS) in 55 patients who underwent temporal lobectomy and were seizure-free postoperatively for >2 years. METHODS: Blinded to clinical details, we reviewed videotapes from video-EEG telemetry monitoring with attention paid to seizure semiology. RESULTS: Useful lateralizing features included unilateral clonic activity (with the seizure focus contralateral in all patients), unilateral dystonic or tonic posturing (with the seizure focus contralateral in 90 and 86%, respectively), unilateral automatisms (with the seizure focus ipsilateral in 80%), and ictal speech preservation (with the seizure focus contralateral to the language-dominant hemisphere in 80%). Versive head rotation occurring < or = 10 s before seizures secondarily generalized consistently predicted a contralateral focus. Seizure manifestations less predictive but suggestive of lateralization included ictal speech arrest and postictal speech status, with predictive values of 67%. Seizure manifestations not providing reliable lateralizing information included eye deviation, type of aura, and versive head movements occurring at times other than immediately before seizures secondarily generalized. CONCLUSIONS: In TLE, several clinical seizure manifestations are useful in lateralizing the seizure focus, although some provide no reliable information. Therefore, ictal semiology can assist in the evaluation of patients for seizure surgery, providing additional information in the lateralization of TLE.

Adolescent↗

Lateral specialization and psychiatric issues: speculations on development and the evolution of consciousness.

At the start of this lecture, I invited you to indulge with me in a "dessert" of speculations. I hope it has been a sufficiency, not a surfeit. In summary, we have examined a hypothetical model of some dissociations of consciousness and the expression of unconscious symptoms in adults; we then explored some possible conditions that would account for the development of separate mental streams. In the course of this exploration we were led to question some basic assumptions about the unity of the self, and we proposed some possible mechanisms by which lateral specialization develops in children. This model of the development of lateral specialization has some implications for the study of evolution of the human brain and consciousness. It would seem useful to examine the relationship between the evolution of the commissural systems and the evolution of different capacities for consciousness. According to this model, the full development of lateral specialization depends upon the later myelination of the commissures, which makes possible the autonomy and competition between hemispheres. By this means, only minimal differences between hemispheres need to be specified genetically, since the rest of lateralization can be produced by progressive differentiation, through interactions with the environment. Thus man's eternal, internal struggle may be the price paid for the evolution of lateral specialization.

Adult↗

Lateralization of bands of noise and sinusoidally amplitude-modulated tones: effects of spectral locus and bandwidth.

Lateralization of narrow bands of noise was investigated while varying interaural temporal disparity (ITD), center frequency, and bandwidth, utilizing an acoustic pointing task. Stimuli were narrow bands of noise centered at octave intervals between 500 Hz and 4 kHz with bandwidths ranging from 50-400 Hz. In a second experiment, lateralization for bands of noise and sinusoidally amplitude-modulated (SAM) tones, whose spectral content was constrained to be no lower than 3.8 kHz, was assessed. Overall, relatively large extents of laterality were obtained from all four listeners for ITDs of low-frequency bands of noise. Increasing the bandwidth of these noises did not yield consistent changes in the extent of laterality across ITDs and listeners. Most targets centered at high frequencies were lateralized near the midline. However, three of the four listeners did exhibit rather large displacements of the intracranial image when the bandwidth of the high-frequency noises was 400 Hz or greater. Interestingly, ITDs within high-frequency SAM tones were relatively ineffective. Thus, it appears that ITDs of relatively wide-band, high-frequency stimuli can mediate rather substantial extents of laterality. However, these effects are highly listener-dependent.

Acoustic Stimulation↗

Dopaminergic agonists and muscarinic antagonists improve lateralization in hemiparkinsonian rats in a novel exploratory Y-maze.

Parkinson's disease (PD) is characterized by the degeneration of nigrostriatal dopaminergic neurons. Its primary clinical symptoms are akinesia, tremor, and rigidity, which usually start from one side, resembling the lateralization in hemiparkinsonian rats having 6-hydroxydopamine-induced unilateral lesion of the medial forebrain bundle. A novel exploratory Y-maze was designed to detect the lateralization of hemiparkinsonian rats in terms of biased turns in the maze. Dopamine agonists levodopa (L-3,4-dihydroxyphenylalanine, 10-30 mg/kg) and apomorphine (0.1-0.3 mg/kg), but not methamphetamine (0.5-2 mg/kg), improved the lateralization in the rat model. However, high doses of the dopamine agonists, 30 and 0.3 mg/kg, respectively, caused small movements in the arms that seemed to parallel the increase in counts per turn in the Y-maze. Interestingly, the muscarinic antagonists trihexyphenidyl and scopolamine improved lateralization moderately, while increasing total turns, an index of locomotive activity. (-)-5-Methyl-10,11-dihydro-5H-dibenzo[a,d]cyclohepten-5,10-imine maleate (MK-801) (0.3 mg/kg), an N-methyl-D-aspartate (NMDA) glutamate receptor antagonist, increased total counts, but did not alleviate the lateralization. The alpha2-adrenoceptor antagonist idazoxan (1 and 10 mg/kg) and 2,3-dihydroxy-6-nitro-7-sulfamoylbenzo(f)quinoxaline (1 and 3 mg/kg), a non-NMDA glutamate receptor antagonist, did not affect any of the indices. These findings suggest that the clinical action of drugs on unbalanced movement in PD could be predicted by measuring their effects on lateralization of the 6-hydroxydopamine-lesioned rat model in this exploratory Y-maze.

Animals↗

Spatial properties of central vestibular neurons of monkeys after bilateral lateral canal nerve section.

Thirty-seven neurons were recorded in the superior vestibular nucleus (SVN) of two cynomolgus monkeys 1-2 yr after bilateral lateral canal nerve section to test whether the central neurons had spatially adapted for the loss of lateral canal input. The absence of lateral canal function was verified with eye movement recordings. The relation of unit activity to the vertical canals was determined by oscillating the animals about a horizontal axis with the head in various orientations relative to the axis of rotation. Animals were also oscillated about a vertical axis while upright or tilted in pitch. In the second test, the vertical canals are maximally activated when the animals are tilted back about -50 degrees from the spatial upright and the lateral canals when the animals are tilted forward about 30 degrees . We reasoned that if central compensation occurred, the head orientation at which the response of the vertical canal-related neurons was maximal should be shifted toward the plane of the lateral canals. No lateral canal-related units were found after nerve section, and vertical canal-related units were found only in SVN not in the rostral medial vestibular nucleus. SVN canal-related units were maximally activated when the head was tilted back at -47 +/- 17 and -50 +/- 12 degrees (means +/- SD) in the two animals, close to the predicted orientation of the vertical canals. This indicated that spatial adaptation of vertical canal-related vestibular neurons had not occurred. There were substantial neck and/or otolith-related inputs activating the vertical canal-related neurons in the nerve-sectioned animals, which could have contributed to oculomotor compensation after nerve section.

Action Potentials↗

Afferent projections to the lateral and dorsomedial hypothalamus in a lizard, Gekko gecko.

Afferent projections to the lateral hypothalamic area and dorsomedial hypothalamic nucleus of the lizard Gekko gecko were studied after applications of wheat germ agglutinin conjugated to horseradish peroxidase. Large applications into the hypothalamus labeled several telencephalic populations not observed after smaller injections. These included the rostrolateral area of the dorsal cortex, a sheet of cells deep to the caudal pole of the lateral cortex, the external amygdala, and part of the dorsal ventricular ridge. Other populations were labeled in the diencephalon, including the supraoptic nucleus and nucleus ovalis; in the medulla the medial reticular area was labeled. Injections into the lateral hypothalamic area labeled neurons in the rostrolateral dorsal cortex, anterior, lateral, and dorsal septal nuclei, the striatoamygdalar area, nucleus accumbens, vertical limb of the diagonal band, nucleus of the accessory olfactory tract, the interstitial, ventral anterior, and ventral posterior amygdalar nuclei, several hypothalamic nuclei, and the posteroventral thalamic nucleus. Labeled brainstem populations included the ventral tegmental area, torus semicircularis, parvocellular and ventral isthmal nuclei, superior raphe, and the solitary nucleus. Injections in the dorsomedial hypothalamic nucleus labeled neurons in the rostral and caudolateral poles of the dorsal cortex, anterior septal nucleus, horizontal limb of the diagonal band, nucleus of the anterior commissure, several hypothalamic areas, the lateral habenula, the posteroventral thalamic nucleus, and cells scattered around the dorsolateral anterior thalamic nuclei. Labeled brainstem populations included the torus semicircularis, ventral tegmental area, superior raphe, parvocellular and ventral isthmal nuclei, and the lateral dorsal tegmental nucleus. The results of these studies are compared with findings in amphibians and mammals.

Afferent Pathways↗

A computational model of lateralization and asymmetries in cortical maps.

While recent experimental work has defined asymmetries and lateralization in left and right cortical maps, the mechanisms underlying these phenomena are currently not established. In order to explore some possible mechanisms in theory, we studied a neural model consisting of paired cerebral hemispheric regions interacting via a simulated corpus callosum. Starting with random synaptic strengths, unsupervised (Hebbian) synaptic modifications led to the emergence of a topographic map in one or both hemispheric regions. Because of uncertainties concerning the nature of hemispheric interactions, both excitatory and inhibitory callosal influences were examined independently. A sharp transition in model behavior was observed depending on callosal strength. For excitatory or weakly inhibitory callosal interactions, complete and symmetric mirror-image maps generally appeared in both hemispheric regions. In contrast, with stronger inhibitory callosal interactions, partial to complete map lateralization tended to occur, and the maps in each hemispheric region often became complementary. Lateralization occurred readily toward the side having a larger cortical region or higher excitability. Asymmetric synaptic plasticity, however, had only a transitory effect on lateralization. These results support the hypotheses that interhemispheric competition occurs, that multiple underlying asymmetries may lead to function lateralization, and that the effects of asymmetric synaptic plasticity may vary depending on whether supervised or unsupervised learning is involved. To our knowledge, this is the first computational model to demonstrate the emergence of topographic map lateralization and asymmetries.

Animals↗

Computational studies of lateralization of phoneme sequence generation.

The mechanisms underlying cerebral lateralization of language are poorly understood. Asymmetries in the size of hemispheric regions and other factors have been suggested as possible underlying causal factors, and the corpus callosum (interhemispheric connections) has also been postulated to play a role. To examine these issues, we created a neural model consisting of paired cerebral hemispheric regions interacting via the corpus callosum. The model was trained to generate the correct sequence of phonemes for 50 monosyllabic words (simulated reading aloud) under a variety of assumptions about hemispheric asymmetries and callosal effects. After training, the ability of the full model and each hemisphere acting alone to perform this task was measured. Lateralization occurred readily toward the side having larger size, higher excitability, or higher-learning-rate parameter. Lateralization appeared most readily and intensely with strongly inhibitory callosal connections, supporting past arguments that the effective functionality of the corpus callosum is inhibitory. Many of the results are interpretable as the outcome of a "race to learn" between the model's two hemispheric regions, leading to the concept that asymmetric hemispheric plasticity is a critical common causative factor in lateralization. To our knowledge, this is the first computational model to demonstrate spontaneous lateralization of function, and it suggests that such models can be useful for understanding the mechanisms of cerebral lateralization.

Algorithms↗

Lateral hypothalamic lesions and norepinephrine turnover in rats.

Animals with lateral hypothalamic lesions lost significantly more weight in the 18 h following this lesion than did sham-operated animals or rats with cerebral cortical lesions deprived of food for the same time period. In the acutely fasted sham-operated animals the turnover of norepinephrine in interscapular brown adipose tissue, heart, and pancreas was slowed but in fasted rats with lateral hypothalamic lesions norepinephrine turnover rates were three- to ninefold faster in all three organs. Exposure to the cold (4 degrees C) significantly increased norepinephrine turnover in the interscapular brown adipose tissue, heart, and pancreas of fasted sham-operated rats, but did not further increase the rate of turnover in lateral hypothalamic-lesioned rats. Rats with lesions in the cerebral cortex responded in a fashion similar to that of the sham-operated animals. Gastric erosions and microhemorrhagic gastric mucosa were observed in five of six acutely fasted rats with lateral hypothalamic lesions whereas all sham-operated rats had a normal appearance of the stomach lining. Animals with lateral hypothalamic lesions made 3 wk earlier also showed an increased rate of norepinephrine turnover in the interscapular brown adipose tissue, heart, and pancreas following an 18 h fast. Rats with bilateral lesions in the paraventricular region of the hypothalamus, however, responded similarly to sham-operated animals with a reduction in the turnover in norepinephrine with fasting and an increase in norepinephrine turnover rate after cold exposure even with fasting. These data suggest that lateral hypothalamic lesions produce an acute increase in turnover of norepinephrine, and that this increased turnover persists for up to 3 wk.

Adipose Tissue, Brown↗

Anatomical reconstruction of the lateral ligaments of the ankle with a gracilis autograft: a new technique using an interference fit anchoring system.

BACKGROUND: Few anatomical and minor invasive procedures have been reported for surgical reconstruction of the lateral ligaments to treat lateral instability of the ankle. Furthermore, there are no standards according to which ligaments should be reconstructed. HYPOTHESIS: A new technique for anatomically reconstructing the lateral ligaments of the ankle using an interference fit anchoring system and determining which ligaments need to be reconstructed according to the results of standard stress radiography of the talocrural and subtalar joints will be effective for treating lateral instability of the ankle. STUDY DESIGN: Case series; level of evidence, 4. METHODS: Twenty-one patients with lateral instability of the ankle underwent surgery using the proposed interference fit anchoring system. Standard stress radiographs of the subtalar joint were performed, and if the talocalcaneal angle was less than 10 degrees , only the anterior talofibular ligament was reconstructed; if there was a 10 degrees or greater opening of the talocalcaneal angle, both the anterior talofibular ligament and the calcaneofibular ligament were reconstructed. RESULTS: In the 17 patients who received only the anterior talofibular ligament reconstruction, the mean talar tilt angle on standard stress radiography of the talocrural joint was 14.5 degrees +/- 1.7 degrees before surgery and 2.6 degrees +/- 0.8 degrees 2 years after surgery (P < .0001). For the 4 patients who had both the anterior talofibular ligament and calcaneofibular ligament reconstructed, the mean talar tilt angle was 16.5 degrees +/- 1.5 degrees before surgery and 3.0 degrees +/- 0.5 degrees 2 years after surgery (P = .0015). The overall mean talocalcaneal angle on standard stress radiography of the subtalar joint was 11.3 degrees +/- 1.4 degrees before surgery and 3.5 degrees +/- 0.8 degrees 2 years after surgery (P = .0060). CONCLUSION: The proposed system has several advantages, including anatomical reconstruction with normal stability and range of motion restored, the need for only a small incision during the reconstruction, and sufficient strength at the tendon graft-bone tunnel junction, in comparison with the tension strength of the lateral ligaments of the ankle.

Adolescent↗

Very slow EEG responses lateralize temporal lobe seizures: an evaluation of non-invasive DC-EEG.

BACKGROUND: This study tested the idea that very slow EEG responses (direct current [DC] potential shifts) could be detected noninvasively during temporal lobe (TL) seizures, and that these shifts give lateralizing information consistent with that obtained by other methods. METHODS: Seven patients with TL epilepsy (TLE) were recorded with scalp DC-EEG technique at bedside. All recordings were performed simultaneously with conventional EEG (scalp in five, and intracranially in two; two patients with scalp recordings were recorded intracranially later). Seizures in five patients originated in the mesial TL. Ictal DC shifts were evaluated by comparing them to the temporal evolution of ictal discharges, and by comparing the laterality of these shifts to the side of seizure onset defined by routine EEG and other presurgical diagnostic tests. RESULTS: All seizures (35/35) were associated with negative DC shifts at temporal derivations (30 to 150 micro V relative to vertex), beginning at the electrical seizure onset, and lasting for the whole seizure. In eight seizures (five patients) with documented mesial TL onset, the polarity of the DC shift was initially positive followed by a negative one after lateral spread of seizure activity. In all cases, the side of the EEG shift agreed with other diagnostic tests, and, at times, was more clearly lateralized than the conventional scalp EEG. CONCLUSIONS: DC-EEG recordings are practical and achievable at the bedside. Ictal DC shifts are consistently observed in scalp recordings in TL seizures, and reliably lateralize them. This method may hold promise in reducing the need for invasive monitoring in patients with TLE where other noninvasive tests are equivocal.

Adult↗

Asymmetry of the lateral (sylvian) fissures in man.

We compared the courses of right and left lateral (sylvian) fissures by superimposing left lateral and reversed right lateral photographic slide projections and tracing the sulci and fissures of each hemisphere in different colors. A characteristic pattern of divergence of posterior regions of the lateral fissures was noted in 25 of 36 adult brains. After pursuing similar courses, the right lateral fissure angulates sharply upward into the inferior parietal area while the left one continues posteriorly. As a consequence, on the right, there is a smaller parietal operculum, a shorter planum temporale, a higher sylvian point, and compensatory expansion of the inferior parietal region posterior to the lateral fissure.

Adolescent↗

Unilateral blinking: a lateralizing sign in partial seizures.

BACKGROUND: Despite lateralizing signs, clinical lateralization of partial seizures may be difficult. We evaluated the usefulness of ictal unilateral blinking as a new lateralizing sign. METHODS: We retrospectively searched our seizure database over a 30-month period and collected videotapes of patients with ictal unilateral blinking. After initial review, we excluded patients in whom blinking was not clearly unilateral and those in whom it was accompanied by simultaneous facial clonic activity or mouth deviation. All patients underwent prolonged EEG-video monitoring. RESULTS: We identified 14 patients who met the above criteria, for a frequency of 1.5%. Age ranged from 18 months to 50 years (mean, 21.6). There were 11 males and 3 females. Unilateral blinking occurred 0 to 37 seconds (mean, 10) after clinical onset and was visible for 1 to 37 seconds (mean, 17). In 10 patients, other lateralizing signs were present. All patients had partial epilepsy, localized by surface EEG in 10 and by additional invasive EEG in four--nine were left hemisphere (four temporal, four frontal, one not further localized), three right hemisphere (two temporal, one frontal), and two undetermined. Of the 12 patients whose epileptogenic zone was lateralized, blinking was ipsilateral in 10 and contralateral in two. The predictive value of unilateral blinking was 83% against EEG localization. CONCLUSION: Unilateral blinking is a relatively uncommon but reliable lateralizing sign in partial seizures, usually indicating an ipsilateral epileptogenic zone.

Adolescent↗

Relative utility of 1H spectroscopic imaging and hippocampal volumetry in the lateralization of mesial temporal lobe epilepsy.

OBJECTIVES: To determine the relative utility of 1H MRSI and hippocampal volumetry for the lateralization of mesial temporal lobe epilepsy (MTLE) in patients with intractable epilepsy. BACKGROUND: MTLE is the most common partial-onset seizure disorder in patients undergoing temporal lobe epilepsy surgery. MR volumetry and spectroscopy are reliable preoperative imaging techniques for the lateralization of MTLE. METHODS: We analyzed the 1H MRSI and hippocampal formation volumes preoperatively in 30 consecutive patients who had undergone temporal lobectomy. RESULTS: Volumetry correctly lateralized the side of surgery in 93% of patients and 1H MRSI did so in 97% of patients. Incorrect lateralization occurred by volumetry in two patients and by 1H MRSI in one patient. Concordance between all MRI modalities was 73%. Pearson's analysis revealed no correlation between the degree of hippocampal volume loss and the creatine-to-N-acetylated-compounds ratio. CONCLUSIONS: Volumetry and 1H MRSI correctly lateralized most patients with MTLE and complement each other in final lateralization. The lack of correlation between the severity of volume loss and the degree of metabolic disturbance suggests that the techniques examine distinct pathophysiologic processes in MTLE.

Adolescent↗

Left-right lineage analysis of the embryonic Xenopus heart reveals a novel framework linking congenital cardiac defects and laterality disease.

The significant morbidity and mortality associated with laterality disease almost always are attributed to complex congenital heart defects (CHDs), reflecting the extreme susceptibility of the developing heart to disturbances in the left-right (LR) body plan. To determine how LR positional information becomes ;translated' into anatomical asymmetry, left versus right side cardiomyocyte cell lineages were traced in normal and laterality defective embryos of the frog, Xenopus laevis. In normal embryos, myocytes in some regions of the heart were derived consistently from a unilateral lineage, whereas other regions were derived consistently from both left and right side lineages. However, in heterotaxic embryos experimentally induced by ectopic activation or attenuation of ALK4 signaling, hearts contained variable LR cell composition, not only compared with controls but also compared with hearts from other heterotaxic embryos. In most cases, LR cell lineage defects were associated with abnormal cardiac morphology and were preceded by abnormal Pitx2c expression in the lateral plate mesoderm. In situs inversus embryos there was a mirror image reversal in Pitx2c expression and LR lineage composition. Surprisingly, most of the embryos that failed to develop heterotaxy or situs inversus in response to misregulated ALK4 signaling nevertheless had altered Pitx2c expression, abnormal cardiomyocyte LR lineage composition and abnormal heart structure, demonstrating that cardiac laterality defects can occur even in instances of otherwise normal body situs. These results indicate that: (1) different regions of the heart contain distinct LR myocyte compositions; (2) LR cardiomyocyte lineages and Pitx2c expression are altered in laterality defective embryos; and (3) abnormal LR cardiac lineage composition frequently is associated with cardiac malformations. We propose that proper LR cell composition is necessary for normal morphogenesis, and that misallocated LR cell lineages may be causatively linked with CHDs that are present in heterotaxic individuals, as well as some 'isolated' CHDs that are found in individuals lacking overt features of laterality disease.

Activin Receptors↗

Lateral eye-movement responses to visual stimuli.

The association of left lateral eye-movement with emotionality or arousal of affect and of right lateral eye-movement with cognitive/interpretive operations and functions was investigated. Participants were junior and senior students enrolled in an undergraduate course in developmental psychology. There were 37 women and 13 men, ranging from 19 to 45 yr. of age. Using videotaped lateral eye-movements of 50 participants' responses to 15 visually presented stimuli (precategorized as neutral, emotional, or intellectual), content and statistical analyses supported the association between left lateral eye-movement and emotional arousal and between right lateral eye-movement and cognitive functions. Precategorized visual stimuli included items such as a ball (neutral), gun (emotional), and calculator (intellectual). The findings are congruent with existing lateral eye-movement literature and also are additive by using visual stimuli that do not require the explicit response or implicit processing of verbal questioning.

Adult↗