Cognitive functions of the temporal lobe in the dog: a review

1 The current paper reviews the role of temporal lobe structures in learning and different kinds of memory, with an emphasis on behavioral tasks that re auditory stimuli. 2 The effects of lesions to structures in the temporal lobe were examined in separate groups of dogs, which were trained on an auditory spatial delayed response, or in a trial-unique auditory delayed match to sample recognition task. 3 Spatial memory was impaired after bilateral hippocampal lesions. On the other hand, neither an anterior temporal lesion or rhinal cortical injury nor combined lesion to the hippocampus and the anterior temporal lobe, affected postoperative retraining and performance of the spatial task. 4 Auditory recognition memory task was not impaired after a hippocampal and/or rhinal cortex lesion. However, postoperative retraining of the task was impaired after a lesion to auditory association areas. 5 These results confirm the role of the hippocampus in spatial memory in the dog. On the other hand, the organization of auditory recognition functions within the temporal lobe appears to be different from those described for visual recognition functions.     

The inferior, anterior temporal lobes and semantic memory clarified: Novel evidence from distortion-corrected fMRI

The neural basis of semantic memory generates considerable debate. Semantic dementia results from bilateral anterior temporal lobe (ATL) atrophy and gives rise to a highly specific impairment of semantic memory, suggesting that this region is a critical neural substrate for semantic processing. Recent rTMS experiments with neurologically-intact participants also indicate that the ATL are a necessary substrate for semantic memory. Exactly which regions within the ATL are important for semantic memory are difficult to detect from these methods (because the damage in SD covers a large part of the ATL). Functional neuroimaging might provide important clues about which specific areas exhibit activation that correlates with normal semantic performance. Neuroimaging studies, however, have not consistently found anterior temporal lobe activation in semantic tasks. A recent meta-analysis indicates that this inconsistency may be due to a collection of technical limitations associated with previous studies, including a reduced field-of-view and magnetic susceptibility artefacts associated with standard gradient echo fMRI. We conducted an fMRI study of semantic memory using a combination of techniques which improve sensitivity to ATL activations whilst preserving whole-brain coverage. As expected from SD patients and ATL rTMS experiments, this method revealed bilateral temporal activation extending from the inferior temporal lobe along the fusiform gyrus to the anterior temporal regions, bilaterally. We suggest that the inferior, anterior temporal lobe region makes a crucial contribution to semantic cognition and utilising this version of fMRI will enable further research on the semantic role of the ATL.     

Semantic knowledge in patient H.M. and other patients with bilateral medial and lateral temporal lobe lesions

We investigated the effects of damage to the medial temporal lobe (MTL) and anterolateral temporal cortex on semantic knowledge. We studied eight male controls, two patients with lesions limited to the hippocampal formation, three postencephalitic patients with extensive MTL lesions and variable damage to the lateral temporal cortex, and patient H.M. (whose lesion is limited mostly to the MTL, but who also has minimal damage to the anterolateral cortex). On 13 tests of semantic memory, patients with lesions limited to the hippocampal formation performed similarly to controls. Postencephalitic patients were mildly to moderately impaired on most tests. Patient H.M.'s performance was impaired on only a few tests and was less severely impaired overall than the three postencephalitic patients. A ranking of test scores showed a direct relationship between impairment and the extent of damage to lateral temporal cortex. These findings, and related findings from other studies, point to the importance of anterolateral temporal cortex for semantic knowledge. Patient H.M. performed uniquely in certain respects. For example, when providing definitions of objects, he made many grammatical errors. In contrast, the other patients with large MTL lesions made no more errors than those made by controls. Considering that H.M.'s lesion, both medially and laterally, is less extensive than the lesions in these other patients, it appears unlikely that his shortcomings in language production are related to his temporal lobe lesion.     

Verbal learning and forgetting in patients with temporal lobe epilepsy

Studies comparing non-surgical patients with left or right temporal lobe epilepsy (TLE) have shown irregular differences in verbal learning and memory. We assessed the performance of unoperated patients with epileptogenic temporal lobe lesions or cryptogenic TLE using a selective reminding procedure for the learning of a word list, and five delayed trials for the recall of learned words. On the selective reminding procedure, patients with left TLE were found to be more impaired than those with right TLE and controls, in agreement with the role of the left temporal lobe in verbal learning. The patients with right TLE were more impaired than the controls, possibly due to the semantic organization of the word list The rate of forgetting learned words was similar in the patient and control groups, suggesting that patients with left TLE can normally retain and/or retrieve stored items. These data support the hypothesis that distinct functional systems subserve learning and memory. Comparisons of the patient subgroups with epileptogenic lesions (hippocampal sclerosis or low-grade glioma) and those with cryptogenic TLE did not reveal any significant difference in learning or in memory, suggesting that epileptiform activity could affect verbal performance as a detectable temporal lesion.     

Semantic memory in partial epilepsy: verbal and non-verbal deficits and neuroanatomical relationships

Semantic memory was evaluated in 124 epilepsy patients, including 84 with left (n=44) or right temporal lobe epilepsy (TLE) (n=40) and 40 with left (n=25) or right frontal lobe epilepsy (FLE) (n=15), in order to determine their verbal and visual deficits, and the neuroanatomical relationships between them. The controls were 35 healthy subjects. Semantic memory was assessed by means of Picture Naming, Picture Pointing, the verbal Pyramid and Palm Trees Test (PPTT), the visual PPTT, Object Decision Hard, and Drawing From Memory. Episodic memory was assessed by means of the Short Story, Rey's Complex Figure, the Verbal and Visual Selective Reminding Procedure and Brown-Peterson Procedure. Factor analysis of the epilepsy patients distinguished their semantic memory scores from other neuropsychological domains. The semantic memory factor was significantly related to the side of the epileptic region, with lower scores in the left hemisphere and left TLE patients. In comparison with the controls, the left TLE patients were significantly impaired on Picture Naming, Picture Pointing, and Object Decision Hard. Subsequent analyses showed that, in comparison with the controls and the right TLE patients, the left TLE patients with lateral temporal lobe lesions were impaired in Picture Naming whereas, in comparison with the controls, the left TLE patients with mesial temporal lobe lesions were impaired in Object Decision Hard. On the contrary, the episodic memory factor was not related to the side of the epileptic region, and a few material-specific tests revealed opposite impairments in the left and right hemisphere patients. These results show that left TLE may cause semantic memory deficits involving verbal and visual information. Unlike the material-specific pattern of episodic memory, this pattern of impairment is in line with the view of an amodal semantic store in which all of the information about a thing overlaps. The semantic memory impairment may reflect damage in the lateral and mesial temporal lobe regions that impair neocortical functions in storing and retrieving information or hippocampal functions in processing meaningful stimuli.     

Memory impairment in humans after bilateral damage to lateral temporal neocortex

The hippocampus and its adjacent medial temporal regions are crucial for episodic memory. However, it is far less obvious whether other temporal regions beyond the medial part are important for memory processing. The memory performance of a group of patients with bilateral lesions over the lateral temporal lobe sparing the hippocampus was assessed and compared with that of patients with relatively spared cortex and patients with bilateral damage to the lateral temporal lobe and the hippocampus. The results demonstrate that bilateral damage to the lateral temporal lobe results in memory impairment across verbal and visual modalities.     

Retrograde memory after unilateral stroke

Over the past two decades, there has been a growing interest in understanding the neural underpinnings of memory of the past. Numerous patients with retrograde amnesia after acute brain damage have been described, but often the causative lesions are bilateral and/or fairly diffuse and one question that has arisen is whether a unilateral lesion is sufficient to cause retrograde memory impairment. In addition, the impact of lesion side and site on the material specificity and temporal extent of retrograde memory deficits has remained unclear. We set out to investigate these issues by comparing 20 patients who had recently had a unilateral stroke that involved (but was not necessarily limited to) either the frontal or temporal lobe to a group of 10 matched normal control subjects on tests of memory of events and semantic details from the autobiographical and public domains. Results indicated that a unilateral lesion was sufficient to cause significant retrograde memory impairment, with right-sided lesions affecting recall of autobiographical events more than left-sided lesions. The memory deficits in these patients were most often relatively mild, but temporally pervasive rather than characterised by a traditional temporal gradient. Furthermore, memory of events (both autobiographical and public) was impaired in patients who had had a stroke that included the hippocampus, but not in those whose strokes spared this region. Finding that patients with mesial temporal lesions had difficulty remembering details related to public events, even when offered recognition choices, raises the possibility that part of their memory storage network (and not just their retrieval abilities) was compromised.     

Recognition and identification of famous faces in patients with unilateral temporal lobe epilepsy.

We examined the performance of 21 patients with unilateral temporal lobe epilepsy (TLE) and hippocampal damage (10 lefts, and 11 rights) and 10 age-matched controls on the recognition and identification (name and occupation) of well-known faces. Famous face stimuli were selected from four time periods; 1970s, 1980s, 1990-1994, and 1995-1996. Differential patterns of performance were observed for the left and right TLE group across distinct face processing components. The left TLE group showed a selective impairment in naming famous faces while they performed similar to the controls in face recognition and semantic identification (i.e. occupation). In contrast, the right TLE group was impaired across all components of face memory; face recognition, semantic identification, and face naming. Face naming impairment in the left TLE group was characterized by a temporal gradient with better naming performance for famous faces from more distant time periods. Findings are discussed in terms of the role of the temporal lobe system for the acquisition, retention, and retrieval of face semantic networks, and the differential effects of lateralized temporal lobe lesions in this process.     

Lexical retrieval and semantic knowledge in patients with left inferior temporal lobe lesions

Background: It has been proposed that anomia following left inferior temporal lobe lesions may have two different underlying mechanisms with distinct neural substrates. Specifically, naming impairment following damage to more posterior regions (BA 37) has been considered to result from a disconnection between preserved semantic knowledge and phonological word forms (pure anomia), whereas anomia following damage to anterior temporal regions (BAs 38, 20/21) has been attributed to the degradation of semantic representations (semantic anomia). However, the integrity of semantic knowledge in patients with pure anomia has not been demonstrated convincingly, nor were lesions in these cases necessarily confined to BA 37. Furthermore, evidence of semantic anomia often comes from individuals with bilateral temporal lobe damage, so it is unclear whether unilateral temporal lobe lesions are sufficient to produce significant semantic impairment.

Aims: The main goals of this study were to determine whether anomia following unilateral left inferior temporal lobe damage reflected a loss of semantic knowledge or a post‐semantic deficit in lexical retrieval and to identify the neuroanatomical correlates of the naming impairment.

Methods & Procedures: Eight individuals who underwent left anterior temporal lobectomy (L ATL) and eight individuals who sustained left posterior cerebral artery strokes (L PCA) completed a battery of language measures that assessed lexical retrieval and semantic processing, and 16 age‐ and education‐matched controls also completed this battery. High‐resolution structural brain scans were collected to conduct lesion analyses.

Outcomes & Results: Performance of L ATL and L PCA patients was strikingly similar, with both groups demonstrating naming performance ranging from moderately impaired to unimpaired. Anomia in both groups occurred in the context of mild deficits to semantic knowledge, which manifested primarily as greater difficulty in naming living things than nonliving things and greater difficulty in processing visual/perceptual as opposed to functional/associative semantic attributes. Lesion analyses indicated that both patient groups sustained damage to anterior inferior temporal lobe regions implicated in semantic processing.

Conclusions: These results contribute to a better understanding of the cognitive mechanism of naming impairment in patients with temporal lobe damage and support the notion that pure anomia and semantic anomia represent two endpoints along a continuum of semantic impairment. Unilateral left temporal lobe lesions in our patients resulted in relatively mild semantic deficits that were apparent primarily in lexical production tasks, whereas severe semantic impairment likely requires bilateral temporal lobe damage.     

Medial temporal lobe structures are needed to re-experience remote autobiographical memories: evidence from H.M. and W.R

The nature and extent of retrograde amnesia in patients with medial temporal lobe (MTL) lesions is currently under debate. While some investigators propose a temporally limited role for the MTL in episodic and semantic memory, others claim that MTL structures are needed for episodic memories of one's entire lifetime, and that only semantic memory becomes independent of the MTL. To address this issue, we tested two amnesic patients, H.M. and W.R., with bilateral MTL lesions on a series of remote memory tests that together distinguished episodic memory from semantic memory performance. Notably, we used a new method to assess autobiographical memory that measured the degree of re-experiencing of personal happenings from the past. Both patients showed relatively spared semantic memory, but severe impairment on measures of autobiographical memory, with no temporal gradient. Our data support the view that MTL structures play a significant role in recalling specific personal episodes, not only from the recent past but from the distant past as well.     

Does the medial temporal lobe bind phonological memories?

The medial temporal lobes play a central role in the consolidation of new memories. Medial temporal lesions impair episodic learning in amnesia, and disrupt vocabulary acquisition. To investigate the role of consolidation processes in phonological memory and to understand where and how, in amnesia, these processes begin to fail, we reexamined phonological memory in the amnesic patient HM. While HM's word span performance was normal, his supraspan recall was shown to be markedly impaired, with his recall characterized by a distinctive pattern of phonological errors, where he recombined phonemes from the original list to form new response words. These were similar to errors observed earlier for patients with specifically semantic deficits. Amnesic Korsakoff's patients showed a similar, though much less marked, pattern. We interpret the data in terms of a model of lexical representation where temporal lobe damage disrupts the processes that normally bind semantic and phonological representations.     

Amnesia following herpes simplex encephalitis]

We describe three patients presenting themselves with amnesia following herpes simplex encephalitis. All three patients showed anterograde amnesia. Moreover, one patient showed retrograde amnesia extending about fifty years prior to the onset of the illness. Two patients revealed semantic memory disorder, disinhibitory behaviors and confabulations, which suggested the existence of frontal lobe dysfunction. MRI of all three patients disclosed uni- or bilateral temporal lesions. SPECT images showed decreased uptake not only in the temporal lobes but also in the frontal lobes. Amnesia following herpes simplex encephalitis has been thought to be caused by the temporal lobe disorder. However, we postulate that the frontal lobe dysfunction might contribute to the appearance of amnesia.     

Semantic memory impairment in temporal lobe epilepsy associated with hippocampal sclerosis

Episodic memory impairment is a well-recognized feature of mesial temporal lobe epilepsy. Semantic memory has received much less attention in this patient population. In this study, semantic memory aspects (word-picture matching, word definition, confrontation and responsive naming, and word list generation) in 19 patients with left and right temporal lobe epilepsy secondary to mesial temporal sclerosis (MTS) were compared with those of normal controls. Patients with LMTS showed impaired performance in word definition (compared to controls and RMTS) and in responsive naming (compared to controls). RMTS and LMTS patients performed worse than controls in word-picture matching. Both patients with left and right mesial temporal lobe epilepsy performed worse than controls in word list generation and in confrontation naming tests. Attentional-executive dysfunction may have contributed to these deficits. We conclude that patients with left and right MTS display impaired aspects of semantic knowledge. A better understanding of semantic processing difficulties in these patients will provide better insight into the difficulties with activities of daily living in this patient population.     

Impairment of semantic memory after basal forebrain and fornix lesion

Semantic memory impairment is classically associated with lesion of the anterior temporal lobe. We report the case of a patient with severe semantic knowledge impairment and anterograde amnesia after bilateral ischemic lesion of the fornix and of the basal forebrain following surgical clipping of an aneurysm of the anterior communicating artery. Fluorodeoxyglucose positron emission tomography (FDG-PET) showed a temporal hypometabolism. Severe semantic impairment is a rare complication after rupture of an anterior communicating artery aneurysm and may result from disconnection of the temporal lobe.     

Autobiographical Memory After Temporal Lobe Lesions

Abstract

To investigate how the brain organizes and stores autobiographical memory, eight subjects with focal lesions of the temporal lobe and one comparison subject with frontal lobe lesion were studied with the Autobiographical Memory Interview (AMI). The AMI surveys both personal semantic memory and autobiographical incidents from childhood, early adulthood and recent life. Left mesial temporal lobe lesion caused anterograde and time-limited retrograde autobiographical memory changes. More extensive left temporal lobe lesion disrupted personal semantic memory dating back to childhood, but did not impair recollection of autobiographical incidents. However, bilateral temporal lobe lesions caused extensive autobiographical memory deficits which varied in temporal extent according to the particular location of damage. Bilateral prefrontal cortex damage also resulted in severe impairment, which appeared to be related to disorganized retrieval. The findings suggest that many verbal-semantic aspects of autobiographical memory are mediated by left temporal structures, whereas autobiographical episodes are more widely distributed and dependent upon interactions of prefrontal cortex with diverse temporal lobe regions.     

A cognitive chameleon: Lessons from a novel MAPT mutation case

We report a case of frontotemporal dementia caused by a novel MAPT mutation (Q351R) with a remarkably long amnestic presentation mimicking familial Alzheimer’s disease. Longitudinal clinical, neuropsychological and imaging data provide convergent evidence for predominantly bilateral anterior medial temporal lobe involvement consistent with previously established neuroanatomical signatures of MAPT mutations. This case supports the notion that the neural network affected in MAPT mutations is determined to a large extent by the underlying molecular pathology. We discuss the diagnostic significance of anomia in the context of atypical amnesia and the impact of impaired episodic and semantic memory systems on autobiographical memory.     

Memory for the temporal order of events in patients with frontal lobe lesions and amnesic patients

Patients with frontal lobe lesions, amnesic patients with Korsakoff's syndrome, other (non-Korsakoff) amnesic patients, and control subjects were given tests of memory for temporal order. In the first experiment, subjects were presented with a list of 15 words and then asked to reproduce the list order from a random array of the words. In the second experiment, they were asked to arrange in chronological order a random display of 15 factual events that occurred between 1941 and 1985. In both experiments, patients with frontal lobe lesions were impaired in placing the items in the correct temporal order, despite normal item memory (i.e. normal recall and recognition memory for the words and facts). The two groups of amnesic patients exhibited impaired memory for temporal order as well as impaired item memory. Patients with Korsakoff's syndrome exhibited poorer temporal order memory than the other amnesic patients, despite similar levels of item memory. These findings demonstrate that patients with frontal lobe lesions have difficulty organizing information temporally. Patients with Korsakoff's syndrome, who have both diencephalic and frontal damage, have memory impairment together with a disproportionate deficit in memory for temporal order.     

Knowing "what" and knowing "when"

The ability to situate autobiographical memories accurately in the "time-line" of one's own life is a particular aspect of retrograde memory that has received little attention in well-controlled, systematic studies. Here, we addressed this issue by testing the hypothesis that patients with basal forebrain damage would be impaired in their ability to place various autobiographical memories accurately on a 'time-line' of their life. Seven such subjects were contrasted with 11 medial temporal lobe subjects, 8 brain-damaged comparison subjects, and 18 normal comparison subjects, using a procedure in which subjects placed autobiographical events on a time-line of their life. The basal forebrain group was very impaired in this task, relative to the other groups, and on average, misplaced events by more than five years. Although the basal forebrain group was also impaired in retrieving the contents of autobiographical memory, they did not differ statistically from the medial temporal lobe group in this regard (and the medial temporal lobe group did not have impaired time placement of memories). The results indicate an intriguing dissociation between "knowing what" and "knowing when," and suggest that the basal forebrain contains structures that are especially important for "knowing when." Our findings are compatible with the view that the basal forebrain participates critically in retrieval strategies important for memory chronology, which contrasts with the medial temporal lobe's critical role in relational memory per se.     

Atypical non-progressive semantic impairment following allogeneic bone marrow transplantation in a patient with Waldenström’s macroglobulinemia: A case report

Objective: A case report of a 74-year-old male presenting with an atypical multimodal semantic impairment. The patient was diagnosed with Waldenström macroglobulinemia (WM) for which he received allogeneic bone marrow transplantation (BMT) due to disease progression. Following BMT, he developed a sudden onset of semantic difficulties that have remained unchanged for eight years. No other cognitive functions have been affected and his activities of daily living remain fully preserved.

Method: The patient was assessed at our neuropsychology unit with six neuropsychological evaluations over an 8-years follow-up period following BMT. Additional semantic tests were administered during the last three evaluations. Four MRI scans (at age 62, 66, 69 and 74) and 18F-FDG PET (at age 74) were obtained.

Results: The patient presents a multimodal semantic impairment, including naming impairment, visual agnosia, prosopoanomia, associative prosopagnosia, topographical disorientation and impaired retrograde memory for public events. MRI scans and 18F-FDG PET revealed bilateral symmetrical atrophy (temporal?>?frontal) and inferior bilateral temporal lobe hypometabolism, respectively. Neuroradiological examination was unremarkable prior to BMT.

Conclusion: Clinical diagnosis remains a challenge given the focal and stable nature of his deficits. We hypothesize that the BMT procedure might have resulted in the temporal lobe damage and subsequent semantic impairment. We recommend obtaining a thorough neuropsychological evaluation of patients who receive allogenic BMT, both prior to and following transplant.     

Memory following intracarotid amobarbital injection contralateral to hippocampal damage

We examined the relationship between memory performance and hippocampal damage in temporal lobe epileptics undergoing the intracarotid amobarbital sodium procedure (IAP). Overall memory performance in the course of IAP was correlated with seizure lateralization. The hemisphere of seizure focus had impaired IAP memory in 63% (19/30) of the patients. The IAP memory performance following perfusion of the hemisphere contralateral to severe hippocampal lesions was impaired in five of six patients. These patients also exhibited hypometabolism of the impaired temporal lobe as determined independently by positron emission tomography. The single patient with a severely damaged hippocampus who did not demonstrate IAP memory impairment with contralateral hemisphere injection did not exhibit perfusion of the ipsilateral posterior cerebral artery with amobarbital. Memory performance following intracarotid amobarbital injection contralateral to a less severely damaged hippocampus was impaired in 14 of 24 patients and was not related to extent of hippocampal damage, temporal lobe hypometabolism of labeled glucose, perfusion of the ipsilateral posterior cerebral artery, hemispheric language dominance, or order of injection. These results indicate that impaired memory performance during IAP may reflect severe hippocampal damage and/or epileptogenic abnormality.