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Visual and Motor Recovery After “Cognitive Therapeutic Exercises” in Cortical Blindness

A Case Study

De Patre, Daniele BS, DPT; Van de Winckel, Ann PT, MS, PhD; Panté, Franca MS, DPT; Rizzello, Carla MS, DPT; Zernitz, Marina DPT; Mansour, Mariam MD; Zordan, Lara PhD; Zeffiro, Thomas A. MD, PhD; O'Connor, Erin E. MD; Bisson, Teresa PT, DPT, NCS, ATP; Lupi, Andrea MD; Perfetti, Carlo MD

Journal of Neurologic Physical Therapy: July 2017 - Volume 41 - Issue 3 - p 164–172
doi: 10.1097/NPT.0000000000000189
Case Studies
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Background and Purpose: Spontaneous visual recovery is rare after cortical blindness. While visual rehabilitation may improve performance, no visual therapy has been widely adopted, as clinical outcomes are variable and rarely translate into improvements in activities of daily living (ADLs). We explored the potential value of a novel rehabilitation approach “cognitive therapeutic exercises” for cortical blindness.

Case Description: The subject of this case study was 48-year-old woman with cortical blindness and tetraplegia after cardiac arrest. Prior to the intervention, she was dependent in ADLs and poorly distinguished shapes and colors after 19 months of standard visual and motor rehabilitation. Computed tomographic images soon after symptom onset demonstrated acute infarcts in both occipital cortices.

Intervention: The subject underwent 8 months of intensive rehabilitation with “cognitive therapeutic exercises” consisting of discrimination exercises correlating sensory and visual information.

Outcomes: Visual fields increased; object recognition improved; it became possible to watch television; voluntary arm movements improved in accuracy and smoothness; walking improved; and ADL independence and self-reliance increased. Subtraction of neuroimaging acquired before and after rehabilitation showed that focal glucose metabolism increases bilaterally in the occipital poles.

Discussion: This study demonstrates feasibility of “cognitive therapeutic exercises” in an individual with cortical blindness, who experienced impressive visual and sensorimotor recovery, with marked ADL improvement, more than 2 years after ischemic cortical damage.

Video Abstract available for additional insights from the authors (see Video, Supplemental Digital Content 1, available at: http://links.lww.com/JNPT/A173).

Centro Studi di Riabilitazione Neurocognitiva, Villa Miari, Santorso, Vicenza, Italy (D.D.P., F.P., C.R., M.Z., C.P.); Divisions of Physical Therapy and Rehabilitation Science, Department of Rehabilitation Medicine, Medical School, University of Minnesota Twin Cities, Minneapolis (A.V.d.W.); Division of Physical Therapy, Department of Rehabilitation Medicine, Medical School, University of Minnesota Twin Cities, Minneapolis (T.B.); Unità Operativa di Neuroradiologia, Vicenza, Italy (M.M.); Unità Operativa Complessa di Neurochirurgia, Vicenza, Italy (L.Z.); Neurometrika, Potomac, Maryland (T.Z.), and Department of Radiology, Temple University School of Medicine, Philadelphia, Pennsylvania (E.O'C.); and Unità Operativa Complessa di Medicina Nucleare, Vicenza, Italy (A.L.).

Correspondence: Daniele De Patre, BS, DPT, Centro Studi di Riabilitazione Neurocognitiva, Villa Miari, Lesina di Sopra, 111, Santorso, Italy 36014 (danieledepatre1@alice.it) or Ann Van de Winckel, PT, MS, PhD, Divisions of Physical Therapy and Rehabilitation Science, Department of Rehabilitation Medicine, Medical School, University of Minnesota Twin Cities, MMC388, 420 Delaware ST SE, Minneapolis, MN 55455 (avandewi@umn.edu).

Daniele De Patre and Ann Van de Winckel contributed equally to this work and shared first authorship.

There is no financial interest or benefit arising from the direct applications of their research. No author or author's employer or sponsor has a financial, commercial, legal, or professional relationship with other organizations, or with the people working with them, that could influence the author's research.

Accepted posters were presented in April 2016 at a local MN-APTA conference and further at the Institute for Engineering in Medicine conference and Wallin neuroscience conference, both of which are internal conferences at the University of Minnesota.

The authors declare no conflict of interest.

Supplemental digital content is available for this article. Direct URL citation appears in the printed text and is provided in the HTML and PDF versions of this article on the journal's Web site (www.jnpt.org).

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INTRODUCTION

Cortical blindness results from damage to the primary visual cortex (V1) or geniculocalcarine pathways.1–3 Damage can result from stroke, brain anoxia during heart surgery, cardiac arrest, or asthma attacks.1,4,5 Electroencephalography (EEG) is used to confirm cortical blindness, when imaging with computed tomography shows no abnormalities.1,4 Recovery from cortical blindness is generally poor: A 50% to 60% chance of spontaneous recovery is seen in the first month after onset—a probability that diminishes greatly after 3 months to practically nil after 6 months.6–8 Cortical blindness is strongly linked with high levels of activities of daily living (ADL) care2,6,7,9 and low levels of life satisfaction.9 Although visual rehabilitation can stimulate brain plasticity,6,10 improvements in visual function with standard therapy after cortical blindness remain specific to the trained stimuli.6,7,11

Visual restitution methods are used to treat visual field deficits, with methods ranging from luminance detection paradigms,12 training on recognizing shapes, colors or moving targets in the blind field,13 and comparing flickering letters or luminance targets between the intact and blind fields.2,14 If recovery is unsuccessful, people learn compensation strategies or receive optical substitution devices.15

The purpose of this case study was to demonstrate the feasibility and potential value of a novel rehabilitation approach, cognitive therapeutic exercises, described for the first time in a person with cortical blindness treated 20 months after injury. This therapy has been described for recovery of the upper limb in stroke16,17 wherein it is referred to as cognitive sensory motor training.

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CASE DESCRIPTION

The subject was a nonsmoking, 48-year-old woman, with typical weight whose past medical concern was an 8-year history of cardiac arrhythmia (ventricular extrasystoles). Informed consent was obtained. The ethical committee of the rehabilitation center Centro Studi di Riabilitazione Neurocognitiva (Villa Miari) approved the study. The time line of events, clinical assessments, and neuroimaging are illustrated in Table 1.

Table 1

Table 1

The subject had a cardiac arrest due to ventricular fibrillation. Cardiopulmonary resuscitation was started 10 minutes after the arrest and continued for 30 minutes. She suffered postanoxic coma, status epilepticus, and protracted stupor. The Glasgow Coma Scale score was E1VtM1: E1 (no eye opening); Vt (intubated); and M1 (no motor response). The Braden Index (range: 6-23) was 11, reflecting a high risk for pressure ulcers, and Barthel Activities of Daily Living Index (Barthel ADL index) score (range: 0-100) was 0, reflecting incontinence and total ADL dependency.

Two days after being admitted, the subject was in coma, with EEG showing continuous generalized paroxysmal abnormalities compatible with status epilepticus. Computed tomographic scan 3 days after the cardiac arrest showed hypoattenuation with loss of gray-white differentiation in the bilateral occipital lobes, secondary to cytotoxic edema caused by hypoxic/anoxic brain injury. A loss of delineation of basal ganglia was seen bilaterally, following cytotoxic edema (Figure 1). A Fluid-Attenuated Inversion Recovery magnetic resonance imaging study done 13 days after cardiac arrest showed edema resolution in the occipital lobes and basal ganglia (Figure 2).

Figure 1

Figure 1

Figure 2

Figure 2

Twenty days after the cardiac arrest, the subject came out of coma and was transferred to a long-term care facility, complaining of vision loss. Examination revealed an inability to direct or maintain gaze to objects or to follow a light. Pupillary light reflexes were normal. She was globally hypotonic and had dysarthria. She was diagnosed with cortical blindness and tetraplegia. If cortical blindness is caused by cardiac arrest, the prognosis is typically poor if the person is older than 40 years or has cognitive impairments 6 months after the onset.6,7,18,19

Standard motor and visual rehabilitation was started 21 days after cardiac arrest. As part of this rehabilitation, the subject participated in training in which she attempted to recognize images of well-defined symbols contrasted against a light background, which were presented on a screen at 60- to 70-cm distance. She also had to visually track moving targets on a computer screen and identify 3-dimensional objects.

Six months after the cardiac arrest, the subject underwent a fluorodeoxyglucose positron emission tomographic study, showing severe bilateral glucose hypometabolism in the occipital and superior parietal cortices. Diffuse slight reductions in glucose metabolism were seen in the left cerebral and cerebellar hemispheres. Glucose metabolism seemed normal in subcortical structures.

Ten months after the cardiac arrest, a second EEG revealed theta mixed with alpha rhythm activity, suggesting cerebral dysfunction. Intermittent photic stimulation with EEG recording investigated anomalous brain activity.20 The testing did not elicit a normal physiologic response of rhythmic activity over the posterior regions of the head during the visual stimulus.21 Hyperventilation was not possible. Excessive eye muscle activity was noted.

Twenty months after her cardiac arrest, the subject began the cognitive therapeutic exercises22,23 rehabilitation program.

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General Presentation

At the start of the cognitive therapeutic exercises program, the subject was unable to maintain eye contact. Visual search was vague, untargeted, and focused only on areas of high light intensity, such as sunlight pouring through the window. She randomly and vaguely identified shapes or colors but could not identify objects. She reported “seeing as through a hole, filled with fog.” Cognitive impairments were related to visual perception and imagery, including difficulty in perceiving, constructing, processing, and remembering visual information. These impairments were apparent when describing items in her room and when describing images from the past. She could not recognize people or watch television.

She was slightly impaired in movement and position sense, in identifying body positions in space, and in identifying textures by touch. She had hypotonia, opisthotonic rigidity, and dyskinesia with frequent, brief involuntary muscle contractions in her neck, head, trunk, and limbs. Impairments were more pronounced on the left side. She used a wheelchair for mobility. She was dependent in basic ADL and required assistance with reaching and grasping objects.

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INTERVENTION OUTCOME MEASURES

Three clinical scales were administered before, during, and after cognitive therapeutic exercises. The “Motor Evaluation Scale for Upper Extremity in Stroke patients” (MESUPES; range: 0-58 points) assessed tone, muscle recruitment, and active upper limb movements.24 Interrater reliability of the MESUPES is high (arm function: intraclass correlation coefficient (ICC) = 0.95; hand function: ICC = 0.97). Change scores of 8 (95% confidence interval) reflect true change.25 The “Barthel ADL index” (range: 0-100 points; minimal clinical important difference26 = 11.4) measured the level of ADL functioning.27 The scale has excellent interrater reliability (weighted κ coefficient, κw = 0.93).28 The “Warwick-Edinburgh Mental Well-Being Scale” (range: 14-70 points; estimated minimal clinical important difference = 3-8 points29) measured aspects of positive mental health.30 Test-retest reliability at 1 week is high (ICC = 0.83).31

To increase the reliability of the scoring, 3 evaluators independently rated the subject. The therapist scored the subject during direct observation and 2 independent evaluators scored the subject on the basis of video recordings. The independent evaluators were unaware which video was taken at which of the 3 times. The videos showed (1) visual performance, (2) walking, and (3) ADL skills and interviews. Motor Evaluation Scale for Upper Extremity in Stroke was assessed on the right arm. An average score was calculated on the basis of the 3 independent assessments for each scale at each time point (Table 2). Tactile sense was assessed in the thumb, index finger, and hand, and scored as 0 (absent); 1 (impaired); or 2 (normal). Identical scoring was used for movement sense of the index finger (proprioception). Moderate to very high reliability was established for this protocol.32 The tests were repeated midterm and at the end of the therapy (Table 2).

Table 2

Table 2

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OUTCOMES ASSESSED BEFORE INTERVENTION

The subject scored 25/58 on the MESUPES, with loss of fractionated movement. She abducted and flexed her right shoulder to 90° and flexed and extended her elbow and wrist. She opened and closed her hand but could not selectively move the fingers. The left shoulder flexed to 45°; the wrist flexed to neutral position; she could not abduct or extend the thumb, nor selectively move the fingers.

The Barthel ADL index score was 20/100: she was continent for bladder and bowel function but ADL dependent. The Warwick-Edinburgh Mental Well-Being Scale score was 34/70, reflecting a low level of well-being, considering the population mean is 51/70.33 Initially, the subject had impaired sensation in the right thumb, left index finger and palm, and absent sensation in the left thumb. Proprioception was impaired in the right wrist and left index finger and absent in the left wrist.

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INTERVENTION

The cognitive therapeutic exercises focused on restoring vision, improving trunk and neck stability, and right upper limb function. Walking was initiated midterm. After 6 months, the left arm therapy was initiated to increase the subject's independence during bimanual tasks. The rehabilitation22,23 consisted of 2 daily sessions of 1.5 hour each, 5 days per week, for 8 months.

The therapeutic goals for recovery of vision were to increase her field of view, recognize people, establish and maintain eye contact, orient in familiar and new environments, and localize and recognize objects in daily life. The therapeutic goals for motor recovery were to improve reaching, grasping, and manipulation of objects in daily life. Both goals were designed to increase ADL independence and were achieved by correlating sensory and visual information. The exercises evolved from movements guided by the therapist, to movements assisted by the therapist, to active movements. Three examples of exercises designed to achieve object recognition, when the person is not yet able to move the arm accurately, are illustrated in Table 3.

Table 3

Table 3

The goals of the exercises were to recognize 2- and 3-dimensional objects and textures of objects. Exercises increased in complexity and encompassed 3 components: First, all exercises contained a cognitive problem. For example, if the person needed to recognize a 2-dimensional object, the cognitive problem was proposed as the following question: “Is the shape that you have felt the same as the one you are seeing now?” The person solved this problem by (1) attending to the provided sensory information through the affected side of the body with eyes closed, (2) processing, (3) retaining, and (4) subsequently comparing this information to what she saw when opening her eyes.

Second, the subject created a perceptual hypothesis. Based on the cognitive problem, she selected relevant features of the object. Before moving, the participant decided which information she could detect from shoulder and elbow movements, and which tactile information she could use, when the fingertip was guided along the edges of the 2-dimensional object in order to answer the question posed previously. This process of selecting relevant information formed the “perceptual hypothesis” as to what was needed to attend.

Third, the perceptual hypothesis was compared with what was actually perceived. While the fingertip was guided along the edges of a shape, the subject created (with eyes closed) a visual image of what she was feeling. This image was remembered and compared with the object she saw when opening her eyes. She decided whether the shape was the same. The therapist gave feedback: If the answer was correct, the therapist continued with another trial or made the exercise more difficult. If the answer was wrong, the therapist let the subject feel both options: the shape that the person had selected and the shape that the therapist had selected. The subject learned to distinguish both shapes by comparing them, in order to visually perceive the shapes better.

The subject attended every therapy session. Only in the first 2 weeks of the rehabilitation did the subject experience fatigue by the end of the session. No adverse effects were reported by the subject or noted by the therapist.

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OUTCOME ASSESSED AFTER INTERVENTION

After 8 months of rehabilitation, the subject maintained eye contact and recognized faces. She substantially improved her visual exploration skills and localized objects in her environment. She correctly described items in familiar and novel locations such as gardens and streets. She recognized objects and described their characteristics in terms of color, shape, size, material, and surface. However, she excluded her most peripheral vision on both sides.

The subject's field of vision was increased to 15 cm × 10 cm. She reported: “I see your whole face up to the chest. It is not like before when I saw you as through a hole.” She described having clearer vision and experienced seeing through “fog” only on rare occasions, which might have to do with light intensity. She described locations and objects from visual memory and even objects she had not seen for a long time. She watched television, read a wall clock, used her mobile phone, reached and grasped objects, and started to read children's books.

The subject improved 23 points on the MESUPES (48/58), meaning that she moved her right shoulder, elbow, and wrist accurately and moved her fingers selectively. She improved 45 points on the Barthel ADL index (65/100), meaning that she ate, groomed, and dressed independently. She transferred between bed and chair with minimal supervision, was continent, and independent in toilet use. She walked more than 50 yards and negotiated stairs with minimal supervision. She improved 23 points on the Warwick-Edinburgh Mental Well-Being Scale (57/70), indicating that she felt self-reliant. Sensation and proprioception recovered in the right hand midterm and in the left hand at the end of the therapy. The Video (see Supplemental Digital Content 2, available at: http://links.lww.com/JNPT/A174) shows the subject's visual and motor function before, midterm, and after therapy.

After 8 months of therapy, the fluorodeoxyglucose positron emission tomography was repeated (Figure 3). Subtraction of images from before and after treatment showed focal increases in glucose metabolism bilaterally in the occipital pole (BA 17), in areas that showed relatively preserved metabolism prior to rehabilitation. In addition, bilateral metabolic increases were seen in the precentral sulcus (dorsal premotor cortex), angular gyrus, and in the left inferior frontal gyrus.

Figure 3

Figure 3

At 1, 3, 6, 12, and 18 months after completion of the rehabilitation, the subject was examined to assess her ability to identify objects based on vision and to assess which ADL she performed. Her condition remained stable and she continued to recognize objects in her environment and to be independent for basic ADL. She reported having difficulties with cooking, typing, and writing.

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DISCUSSION

In an individual with severe cortical blindness and tetraplegia, we evaluated the impact of a rehabilitation program, cognitive therapeutic exercises, which correlates sensory and visual information to reconstruct vision and improve daily life motor performance. After therapy, the subject recognized objects and identified the characteristics. She recognized people, watched television, read a wall clock, and started to read. She also made an impressive recovery in motor function, ADL, and well-being. She moved her right arm freely and independently moved her fingers. She regained basic ADL independence and walked with minimal supervision. She felt more self-reliant and reported:

I have my life back and I am very happy with this recovery because I do not have to rely on others to do anything. I did not think I would improve after such a long time and recommend this therapy.

This is the first study demonstrating a clinically meaningful improvement in vision and motor function, transferable to daily life functioning more than 2 years after onset of ischemic cortical blindness. It confirms earlier suggestions that visual neuroplasticity can be induced at later stages.6,10 It is unlikely that these clinical results are due to natural recovery, since the standard visual rehabilitation previously received resulted in limited visual recovery, and without ADL improvements. There is no evidence that visual rehabilitation has delayed effects.

Two hypothesized mechanisms are put forward on how cognitive therapeutic exercises enhanced visual recovery. First, metabolism increased in areas spared by the injury, which confirmed earlier findings.7,34 Second, triggering cognitive processes associated with comparing sensory and visual object information could access an alternative route to stimulate preserved occipital areas, presumably from functionally connected parietal and extrastriate areas.

One case study in a subject with noncongenital blindness reported a subjective feeling of seeing lines, following passive tactile stimulation and repetitive transcranial magnetic stimulation (rTMS).35 Conversely, the parietal connectivity network in individuals with congenital blindness, compared with subjects with normal sight, showed functional connectivity between occipital regions, inferior parietal regions, and the anterior intraparietal sulcus (IPS).36 Thus, the parietal cortex provides information to the visual cortex in people with congenital blindness.36 Moreover, both the superior and inferior parietal cortices are involved in processing of spatially coded information from multimodal sensory inputs.36,37 This provides support for functional neuroplasticity in the superior parietal cortex found in our study and its possible association with the tactile spatial discrimination tasks given in therapy.

In adults with normal sight, connections between the somatosensory cortex, through posterior parietal regions, to the human motion area V5/middle temporal complex (MT+) in the extrastriate cortex process visual and tactile motion information.38–40 Tactile input received in the postcentral gyrus influences the visual cortex via back projections through the posterior parietal cortex, intraparietal lobe (IPL), and IPS.41,42 Such back projections are crucial for spatial attention.41,43

The lateral occipital cortex is active during multimodal matching of geometrical shapes of objects, through visual and tactile shape discrimination.38,44–48 Bilateral interactions between the postcentral gyrus, IPS, and lateral occipital cortex have been proposed for haptic shape-selective regions47; between the premotor cortex and IPS for whole object identification38; and in the extrastriate body area for extraction of information regarding the body.49 Texture matching activates inferior frontal areas.44 Overlapping areas between texture and shape discrimination encompass the bilateral angular gyrus, precentral gyrus, and V1.44

The occipital cortex, especially the Lateral Occipital Complex tactile-visual region, is active when touch is used for shape recognition.50 Touch may serve as an additional channel—the “eyes in the fingers”50—providing details about space and time to create a “whole” visual representation.

The main steps to produce visual imagery based on sensory information include having the ability to3 (1) select relevant characteristics necessary to construct a visual image; (2) access visual information stored in long-term memory; (3) generate a visual image; and (4) activate short-term visual memory in order to compare, during the cognitive therapeutic exercises, what is felt with what is seen.22 Some people with cortical blindness experience loss or impoverishment of visual imagery, while others maintain the ability to visualize images.3,51

Initially, the subject had difficulty constructing a mental image of an object and could not remember images from the past. With training, she reconstructed visual images related to present stimuli and described images from the past. Pilgramm et al52 demonstrated that premotor cortex and parietal sensorimotor areas (IPS, IPL, and superior parietal lobe) represent the content of motor imagery. The activity patterns differed depending on which type of action was imagined, that is, aiming, squeezing, or extension-flexion movements with the hand. The same areas were activated during kinesthetic motor imagery.53

In our study, we found increased glucose metabolism in bilateral dorsal premotor areas and angular gyri. This confirms earlier functional magnetic resonance imaging results in passively guided shape and length discrimination tasks with eyes closed,54,55 where discriminating different types of shapes (length; triangles/squares; quadrilaterals) activated different spatial patterns in the frontoparietal cortex. During single neuron recording in the human superior parietal lobe and IPS,56 2 mostly separate neuron populations showed either visual or motor-imagery–related activity during a task that required identification of a cue and imagining performing a corresponding hand shape. We emphasize these findings because we hypothesize that it is important to include several types of sensory-visual comparisons in the rehabilitation program to access the highest potential for visual and sensorimotor recovery.

Lee and Baker38 postulate that the ability to maintain a mental representation is not only restricted to the visual cortex but that other cortical regions can be recruited, depending on the nature of the presented information. For example, frontoparietal areas, related to sensory attention and motor behavior, can maintain representations of spatial position of moving elements, in addition to V1.

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LIMITATIONS

The subject's involuntary muscle contractions in muscles of the neck and the head precluded the ability to perform functional magnetic resonance imaging studies and quantitative visual field examinations. Therefore, the reported visual field deficits were assessed clinically: the subject focused on a red dot in the middle of a frame (45 × 45 cm, 33-cm distance). She had to identify where and when a moving red dot was coming into her field of view and where and how many letters (0, 1, or 2) were added. Eye fixation on the red dot was monitored. During positron emission tomography, the head was comfortably immobilized with a cushioned helmet and strap system. The subject's degree of involuntary head movement was qualitatively similar before and after the intervention, suggesting similar reduction in regional activity in both scans. In addition, inspection of the reconstructed images suggested that head motion was not excessive during imaging.

The subject regained sharper vision and a larger field of view and consistently recognized shapes and colors after 2 months. However, 8 months of 2 daily rehabilitation sessions of 1.5 hour each, 5 days per week were needed to obtain the totality of clinical improvements mentioned previously. Most standard therapies for visual rehabilitation in the United States encompass 6 to 8 months, at least 1 hour a day. Therefore, the proposed therapy is feasible in current routine practice. Nevertheless, further studies are needed to evaluate dosage and intensity for a larger population.

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SUMMARY

This case study demonstrates feasibility and benefits of a novel rehabilitation approach, cognitive therapeutic exercises, in cortical blindness. The subject, diagnosed with cortical blindness and tetraplegia after cardiac arrest, experienced an impressive clinical recovery in visual and motor function, ADL, and well-being. This rehabilitation approach is an alternative to current visual training therapies and therefore informs clinical practice. Further studies, combining structural and functional brain imaging with clinical assessments, are needed to evaluate the mechanisms of this approach and to expand knowledge of mechanisms of vision recovery.

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ACKNOWLEDGMENTS

The authors thank the subject; the speech therapists Anna Maria Boniver and Francesca Leonardi; the physical therapists Mauro Cracchiolo, Marc Aureli Piqué, Marta Ferrer Davesa, and Clara Rizzo for their assistance and comments on the manuscript; and Marina Mazzetto for her advice on the positron emission tomographic data analysis.

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Keywords:

cognitive; PET; plasticity; sensorimotor; vision

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