Introduction. Secondary alterations of executive functions occur in brain injuries together with the primary neuropsychological symptoms, irrespective of the location of the damage and the affected neural networks. Such secondary alterations of executive functions in the presence of language alterations, which is the most frequent primary neuropsychological alteration, in addition to exacerbating the linguistic processing deficit, may be associated to multiple factors inherent to the brain injury or the injured patient. Purpose. To describe the secondary neuropsychological alterations of executive functions in elderly patients with low education levels with acquired language disorders and determine general factors of the injury and of the injured patient ( etiology, location, time of recovery from the injury, age, education level), associated to such secondary alterations of the Attentional Control System. Patients and Methods. The study was conducted on 68 elderly patients with a low education level with language acquired disorders, of both sexes, ranging between 60 and 80 years of age. The executive functions explored included cognitive flexibility, impulsivity control and inhibition of irrelevant automatisms, with the Trail Making Test, the Porteus Maze Test and series of loops. Statistical processing involved a Distribution of Frequencies and Multiple Ordinal Regression. Results and Conclusions. The statistical analysis found secondary neuropsychological alterations of the executive functioning in the elderly patients with language disorders of the study that are associated to the location and the time of recovery from the injury and are irrespective of age, education level and etiology of the injury.
Multiple neuropsychological alterations of varying severity and depth occur in the presence of brain injury, which affect several processing subsystems of the cognitive system. Cognitive neuropsychology differentiates such alterations into primary and secondary alterations [
Primary alterations result from a direct damage to the processing components and mechanisms of the subsystem that exhibit the symptoms. In secondary neuropsychological alterations, the impairment exhibited by a processing subsystem is an indirect result, whether from the impairment of the damaged subsystem or from compensation mechanisms set in motion by the cognitive system in an attempt to reorganize cognitive function after the brain injury [
The secondary alterations that appear after a brain injury usually accompany the primary neuropsychological alterations and respond to the clinical and topographical nature of the primary injury [
This appearance of secondary alterations of the attentional mechanisms and executive functions that occurs in the presence of every brain injury, takes place because the destruction of cognitive automatisms occurring in brain injuries increases the demand for processing and executive control resources for implementing conducts that used to be performed automatically. This implies increased consumption of attentional resources to regulate behavior [
According to Moscovitch [
The selection of information implies the selection, maintenance and disconnection of relevant information and inhibition of irrelevant automatisms. Both operations demand cognitive flexibility that allows alternating between more than two tasks. While executive control implies controlling impulsivity and controlling execution of the Cognitive System’s plans and goals [
Starting from these mechanisms of executive functions, cognitive neuropsychology suggests that their alterations are expressed as deficits, both to activate and disconnect information and maintain the cognitive flexibility required to alternate the attentional focus, as well as to inhibit automated routines that tend to prevail and respond in a planned, voluntary way to situations in the environment that demand immediate attention [
In the case of acquired language alterations, secondary alterations of executive functions exhibit singular clinical characteristics due to the manner in which cognitive function is compromised. Acquired language alterations are usually a consequence of cerebrovascular accidents or traumatic brain injury, pathologies that damage broad brain areas [
The secondary alterations of executive functions exhibited by patients with acquired language alterations hinder the allocation of resources for linguistic processing and optimal distribution between verbal representations and operations active at each moment. This affects the selection of relevant verbal information and inhibition of the irrelevant, evaluation of the linguistic processing needs and allocation of the resources required to maintain the necessary linguistic representations and operations active in the verbal working memory [
However, despite the implications of secondary alterations of executive functioning for patients with acquired language alterations, research on the matter is scarce. In fact, few studies address the alterations of the different executive functions in the presence of brain injury and their possible relation with general factors of the lesion and its consequences to the patients’ Cognitive System functioning.
In the literature, studies of executive functions refer to their specific character in psychiatric or neurological illnesses [
In this context, one could ask, what alterations of executive functions appear in elderly patients with a low education level with acquired language alterations? Is there a relation between general factors of the lesion and of the injured patient, and alterations of executive functions? What general factors of the lesion and of the injured patient are associated to alterations of executive functions in elderly patients with a low education level with acquired language alterations? This article attempts to answer these questions. It is written with the purpose of describing executive functions alterations (cognitive flexibility, impulsivity control and inhibition of irrelevant automatisms) exhibited by elderly patients with a low education level with acquired language alterations, and determining general factors of the brain lesion and of the injured patient (damage etiology, location of lesion, time of recovery from the damage, age and education level) associated with such executive functions alterations.
A cross-sectional descriptive-correlational study was conducted from May through December 2015, in the Language Pathology consult of the “Centro de Estudios de Neurociencias y Procesamiento de Imágenes y Señales” of Universidad de Oriente. This study included in a consecutive way, the 68 elderly patients with acquired language alterations secondary to brain injury that fulfilled the following selection criteria: between 60 and 80 years old; intact motor function of upper limbs, visual-spatial coordination and sensory capacities; no history or clinical evidence of mental confusion, psychopathological disorders, mental deficit disorder or neurodegenerative symptoms; informed consent for taking part in the research.
Each work session took place with the exclusive presence of the evaluator and the evaluated person, who was controlled for the possible presence of neuropharmaceuticals or other variables that could affect test performance.
Two hypotheses were assumed in the research: 1) “Elderly persons with acquired language alterations resulting from brain injury exhibit secondary alterations of cognitive flexibility, impulsivity control and inhibition of irrelevant automatisms, that reach different levels of severity and depth;” 2) “The secondary alterations of cognitive flexibility, impulsivity control and inhibition of irrelevant automatisms displayed by elderly persons with acquired language alterations resulting from brain injury are associated to the etiology of the lesion, the topographical location of the lesion, the time of recovery from the brain damage, age, and education level.”
Verification of these hypotheses implied consideration of the variables: age (60 - 70 years, 71 - 80 years), education level (illiterate, taught to read and write, unconcluded primary, concluded primary, unconcluded secondary), etiology of the lesion (vascular, trauma, tumoral), topographical location of the lesion (anterior, posterior, anteroposterior), time of recovery from the damage (1 - 6 months, 7 - 12 months, 13 - 18 months), cognitive flexibility (adequate, deficit, disruption), impulsivity control (adequate, deficit, disruption) and inhibition of irrelevant automatisms (adequate, deficit, disruption).
The data to confirm the hypotheses were obtained with the following tests:
・ Trail Making Test B. Explores cognitive flexibility. It consists in the graphical execution of a verbal series that alternates two automated series. The subject must alternate between consecutive numbers and letters, enclosed in circles and randomly distributed over a sheet of paper. Grades are reported as the number of seconds required to execute the task. It is graded based on age and education level, and taken to a scale of 0 - 4 points. 0 (more than 93 seconds): pathological performance, 1 (from 69 to 93 seconds): Border Line performance and 2 - 4 points (less than 68 seconds): normal performance [
・ Porteus Maze Test. Explores impulsivity control. Consists in the execution of 10 mazes, where the first 7 have 2 solution opportunities and the last 3 have 4. A line must be traced from a starting point to an exit without lifting the pencil. Test scoring takes into account how participants coped with the Test. Failure in executing a maze implies failure in coping. Adequate coping of all mazes: regular performance. Failure in coping in one or two non-consecutive mazes: Border Line performance. Failure of coping in two consecutive or more than two non-consecutive mazes: pathological performance [
・ Series of Loops. Assess inhibition of irrelevant automatisms. Consists in the execution of a series of loops. Grading is done based on calculation of the test’s Execution Index (IE), for which is considered the total of loops executed (be) and errors in execution (ee). IE = 100 × (ee/be). The value of IE can range between 0 and 100. IE between 0 - 16: regular performance. IE between 17 - 25: Border Line performance. IE > 25: pathological performance [
Once the population of the study was selected and the necessary data obtained, the tests to explore executive functions were administered. This was followed by data analysis and statistical processing with computer program SPSS. First, Frequency Distribution was implemented to verify the first hypothesis; this was followed by implementation of Multiple Ordinal Regression, with 0.05 significance and a 95% confidence interval to verify the second hypothesis.
64.7% of the 68 patients that comprised the study population for this research were male and 35.3% were female.
Average age was 72.3 years, with an age range from 60 to 80 years. Reported age for 41.2% of patients ranged between 60 and 69 years, while 58.8% reported ages between 70 and 80 years.
Education level for 20.6% of patients was unfinished secondary. 14.7% of the cases reported completed primary level, 38.2% reported uncompleted primary level, 14.7% reported having been taught to read and write and 11.8% reported being illiterate.
As to etiology of the brain lesion, in 61.8% of patients it was a vascular lesion (in 50.0% of subjects it was an ischemic vascular lesion and in 11.8% it was of the vascular hemorrhagic type). Trauma etiology was reported in 26.5% of total patients and 11.8% of the cases reported neoplastic etiology.
The topographic location of the brain lesion, in 52.9% of patients was located in the posterior cortex (occipito-parieto-temporal) of the left hemisphere. In 35.3% of patients, the lesion was located in the anterior cortex (frontal) of the left hemisphere. While in 11.8% of the cases, the lesion affected anterior and posterior cortical structures (frontal and temporoparietal essentially) of the left hemisphere. None of the cases reported right or bilateral location of the brain damage.
Time of recovery from the brain damage of total patient’s ranges between 1 and 17 moths. The average time of recovery from the brain damage is 8.1 months, being higher in 50.0% of the study population; 35.3% of the patients recorded damage recovery periods between 1 and 6 months; 44.1%, recorded recovery periods between 7 and 12 months, and 20.6% recorded recovery periods between 13 and18 months.
Cognitive flexibility was adequate in 14.7% of patients (regular performance in the Trail Making Test). 50.0% of the cases recorded cognitive flexibility deficit (Border Line performance in the Trail Making Tests). While, the 35.3% of the cases, exhibited cognitive flexibility disruption (pathological performance in Task B of the Trail Making Test).
Impulsivity control was adequate in 32.4% of patients (regular coping in the Porteus Maze Test). 32.4% of the cases recorded impulsivity control deficit, (Border Line coping in the Porteus Maze Test). While, 35.3% of the cases exhibited impulsivity control disruption (pathological coping in the Porteus Maze Test).
Inhibition of irrelevant automatisms was adequate in 35.3% of the patients (Regular Execution Index in the Series of Loops). 26.5% of the cases recorded inhibition of irrelevant automatisms deficit (Border Line Execution Index in the Series of Loops). While 38.2% of the cases exhibited inhibition of irrelevant automatisms disruption (Pathological Execution Index in the Series of Loops).
As shown in Tables 1-3, the estimation of parameters in the Multiple Ordinal Regression implemented, with probabilities associated to the test > 0.05 (p > 0.05), with a 95% confidence interval, enable us to assume that the factors: age, education level, and etiology of the lesion, are not associated to alterations in cognitive flexibility, control of impulsivity and inhibition of irrelevant automat-
Factor | Estimation | IC (95.0%) | Wald | P |
---|---|---|---|---|
Age | 1.842 | 6,12; −2,43 | 0.71 | 0.391 |
Grade level | 3.17 | −2.94; 9.15 | 1.01 | 0.314 |
Etiology of Brain Injury | 2.54 | −4.91;10.03 | 0.44 | 0.504 |
Topographic localization of injury | −17.78 | −11.90; −2.86 | 35.19 | 0.001 |
Time of Recovery from the Brain Damage | 9.84 | 17.49; 2.18 | 6.35 | 0.012 |
Adjustment to the model = 26.46 |
Factor | Estimation | IC (95.0%) | Wald | P |
---|---|---|---|---|
Age | 1.58 | −5.33; 8.55 | 0.21 | 0.653 |
Grade level | 5.38 | −1.96; 12.74 | 2.06 | 0.151 |
Etiology of Brain Injury | 5.12 | −1.42; 11.67 | 2.35 | 0.125 |
Topographic localization of injury | 22.41 | 40.13; 4.69 | 6.14 | 0.013 |
Time of Recovery from the Brain Damage | 18.77 | 5.93; 31.62 | 8.20 | 0.004 |
Adjustment to the model = 0.00 |
Factor | Estimation | IC (95.0%) | Wald | P |
---|---|---|---|---|
Age | 4.61 | −15.26; 6.04 | 0.72 | 0.396 |
Grade level | 16.01 | 32.14; 0.12 | 3.78 | 0.054 |
Etiology of Brain Injury | 7.12 | −14.92; 0.67 | 3.21 | 0.073 |
Topographic localization of injury | 27.91 | −50.58; −5.23 | 5.81 | 0.011 |
Time of Recovery from the Brain Damage | 27.90 | 5.23; 50.58 | 5.81 | 0.016 |
Adjustment to the model = 0.00 |
isms exhibited by patients with acquired language alterations. While the probabilities associated to the test < 0.05 (p < 0.05), with a 95% confidence interval, allow us to assume that: location of the lesion and time of recovery from the brain damage, are associated to alterations in cognitive flexibility, control of impulsivity and inhibition of irrelevant automatisms exhibited by patients with acquired language alterations studied.
As explained in the introduction of this article, suffering brain damage implies, in addition to generating a primary neuropsychological syndrome, the loss of numerous processing resources of the Cognitive Systems and destruction of a series of automatisms that are executed normally without consumption of cognitive resources. This results in that conducts that were automatically implemented, start demanding processing resources and attention control. All of this greatly reduces the limited resource fund of the Cognitive System [
This condition implies that in the presence of any brain lesion that does not affect the structures supporting executive functions, it is common, together with the primary neuropsychological syndrome, that a pattern of secondary attention alterations appears in the executive functions [
As suggested by Moscovitch [
Based on this functioning of executive functions (included within their information selection and executive control functions), cognitive neuropsychology assumes that the most significant alterations of this attentional component are expressed in the capacity to activate relevant information and its disconnection when it stops being relevant; in maintaining the cognitive flexibility required to alternate the attention focus between two or more stimuli; in the inhibition of strongly automated routines that tend to prevail; and in the capacity for controlled, planned, voluntary response to stimuli or surrounding situations, that demand attention and automatic and impulsive reaction [
The clinical characteristics exhibited by these forms of alteration of executive functions, when expressed as secondary to a primary neuropsychological syndrome, will arise from the dynamic interaction among the alterations of the primary syndrome themselves (which are in turn worsened by the secondary alterations of executive functions) and factors inherent to the brain lesion and the injured patient [
Hence, as shown in the analysis of results, the severity and depth of executive functions alterations secondary to acquired language alterations, reflect a significant inter-individual variability, associated, as shown by the statistical findings of this research, to the time of recovery from the brain lesion and the topographical location of the lesion.
These secondary alterations of executive functions, as noted by Omar-Martinez [
In the case of cognitive flexibility, performance of elderly adults with low education level with acquired language alterations in the Trail Making Test reveals frequent alterations, with varying severity and depth levels. This, assuming Omar-Martinez criteria [
Cognitive flexibility deficit appears as a difficulty to displace the attention focus on information that is no longer relevant, towards the new relevant information. In this case, the subject slowly alternates the attention focus between its active goals, which it reaches with much difficulty, or is barely able to complete just one of them [
Although in the studied patient population both forms of altered cognitive flexibility were recorded, there was marked presence of cognitive flexibility deficit. A large part of patients, even though they exhibited difficulty in executing the task and recording prolonged execution times, were able to complete the established goals. This indicates they were able to allocate sufficient processing resources to attain, although in a longer time, the goals established by the test. These difficulties are also linked to the unspecified slowness exhibited by patients with brain damage, which makes them demand more than subjects with an intact brain, to execute any type of task that implies cognitive effort [
Patients that recorded cognitive flexibility disconnection, in addition to exhibiting rigid, determined behaviors, were unable to adequately complete the test task. In these patients, together with impairment of cognitive flexibility, were recorded damage recovery times under 6 months and anterior or anteroposterior location of the brain lesion.
Patient execution of the Porteus Maze Test reveals frequent alterations in terms of impulsivity control, with varying severity and depth levels, which assuming Omar-Martinez Criteria [
Impulsivity control deficit implies that patients have difficult responding in a voluntary, control, planned way to stimuli or surrounding situations that require automatic and impulsive attention and reaction. These alterations are expressed whether due to failure during an assessment of the attention-demanding situation and determination of an adaptive response, or to difficulties in controlling automatic, impulsive attention during the time in which the situation is valued in order to voluntarily assume a certain determination [
In impulsivity control disconnection, before stimuli or surrounding situations that demand attention and automatic reaction, an impulsive, involuntary, unplanned conduct [
Although both types of impulsivity control alteration were recorded for the patient population with acquired language alterations, the number of patients exhibiting impulsivity control deficit is much higher than the number of patients exhibiting impulsivity control disconnection.
The severity and depth of the impulsivity control alterations exhibited by the patients with acquired language alterations, as shown by the statistical findings, are associated to the time of recovery from the brain lesion and its topographical location.
Taking this into account, it was expected that a parietal location of the lesion implied an aggravation of the alterations for maze execution. The task of the test, in addition to recruiting structures in the prefrontal area of the brain, based on impulsivity control and strategic planning, demands visual-spatial functions that essentially recruit parietal structures [
In the inhibition of irrelevant automatisms, execution exhibited by the patients in the Series of Loops, reveals frequent alterations with varying severity and depth levels, which assuming Omar-Martinez Criteria [
The fundamental characteristic of irrelevant automatisms inhibition deficit is that the subject, in the presence of situations similar to those in which it acquired strongly automated routines (which tend to prevail), exhibits difficulty inhibiting them, barely attaining or with much difficulty, implementation of the relevant conduct [
While in irrelevant automatisms inhibition disconnection, the subjects are unable to inhibit automated routines that tend to prevail during performance of a task [
Both ways of irrelevant automatisms inhibition alterations are present in the patient population. However, as with cognitive flexibility and impulsivity control, patients that exhibit irrelevant automatisms inhibition deficit prevail.
These patients exhibited difficulty in inhibiting the automated routine during task execution, but although it demanded much effort, they were able to adequately implement the relevant conduct. This type of situation, as has already been mentioned, is common in the neuropsychological patient where the brain damage causes global slowness of the cognitive function [
In the cases where inhibition of irrelevant automatisms disconnection was registered, the exhibited performance was distinctly pathological, as none of the patients was able to attain the relevant conduct.
In all the cases, as shown in the analysis of results, the best executions were reported in patients with posterior location of the brain lesion. Those cases with anterior location of the lesion that exhibited scarce alterations in the inhibition of irrelevant automatisms, exhibit prolonged times of recovery from the brain damage. It is therefore assumed that this factor lessened the involvements implied for functioning of the executive functions, damage in the anterior region of the brain, due to the limitations this type of lesion imposes on the Cognitive System’s resource fund [
Nevertheless, it is important to value that the reported frontal damages, in addition to having been registered around the Drill area and showing different levels of topographical extension, in none of the cases directly affected frontal structures that, as assumed by authors like Moscovitch and Umiltà [
The proven fact, based on the statistical findings obtained by means of the Multiple Ordinal Regression implemented in the research, of the connection between the topographical location of the lesion and the time of recovery from the brain lesion, with secondary alterations of the patient’s executive functions during performance of the administered neuropsychological tests, is entirely consistent with what has been presented thus far, as well as the fact that age, education level and etiology of the lesion are not associated to the exhibited patient executive functions alterations.
From a neuropathology perspective, a lesion’s topographical location, in general, is a neurological factor that by its own essence is associated to a large part of the characteristics shown by the neuropsychological alterations exhibited by patients with brain damage. On this factor depends the neural networks affected by the lesion, which directly or indirectly determine the primary neuropsychological alterations, as well as the areas to be affected due to the effect of diaschisis, which give rise overall, to the secondary neuropsychological alterations [
The functional organization of the brain implies that specific brain areas are going to be recruited in a more or less defined way for the implementation of specific psychological functions. The cortical regions of both brain hemispheres, which are essentially responsible for cognitive function, are divided structurally and functionally, by the Central sulcus. From this, afferent processing of information takes place in the posterior regions of the cortex and efferent processing and mental control of activity (including executive functions) takes place in the anterior regions. This causes that secondary alteration that will be manifest in the functioning of executive functions in presence of a focal lesion, will be mediated by the anterior or posterior location of the lesion (in addition to being associated to the alterations inherent to the primary syndrome.) General physiopathology of the damage and the amount of processing resources and cognitive automatisms lost will depend on the location [
In frontal lesions, secondary affectation of executive functions function must be, therefore, more distinct and exhibit greater severity and depth than in parieto-temporo-occipital lesions. This because cognitive functions supported by frontal brain circuits make the greatest demand for processing resources from the Cognitive System [
The time of recovery from the brain damage, defined as the period elapsed since the patient sustained the lesion until the time he is subject to the neuropsychological assessment [
Hence, recovery from the physiopathological conditions caused by brain injury and the brain’s capacity to modify functions and compensate damages has proven to play an important role in the recovery of cognitive functions and processing resources after brain damage [
The brain plasticity at the core of matters linked to the time of recovery from brain damage expresses the nervous system’s adaptive capacity to minimize the effects of lesions through a structural and functional reorganization of the brain [
This factor is significantly associated to how the patient will perform in the different neuropsychological tests it will be subject to, as well as its adaptation to its disability and compensation of its deficits. These peculiarities that have been argued are reflected in the results obtained in this research, where the most compromised executions of the different functioning of executive functions are encountered in patients with the shortest recovery time from the brain injury.
Omar-Martinez, E., Pino-Melgarejo, M., Idárraga-Cabrera, C. and Rodríguez-Aldana, Y. (2017) Performance-Associated Factors of Elderly Patients with a Low Education Level, with Acquired Language Alterations in Tests to Explore Ex- ecutive Functions. World Journal of Neuroscience, 7, 293-306. https://doi.org/10.4236/wjns.2017.73025